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Is there evidence that some non-human species perform sexual selection based primarily on intelligence? How do they do this?

Is there evidence that some non-human species perform sexual selection based primarily on intelligence? How do they do this?


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I'm a biology amateur, but it seems like sexual selection is almost always performed based on physical characteristics, the outcome of physical contests, or some sort elaborate courtship. But do any non Homo-Sapiens perform sexual selection based on intelligence factors, like problem solving abilities? If so, how does the species accomplish this? I know natural selection as a whole would definitely favor intelligent individuals, but I'm curious if any species actually takes this into account when choosing mates.


Very intresting question. The problem is that animal intelligence is hard to measure not only for scientists, but probably also for the potential mate. Paradoxically, that is why selection for intelligence, if it occurred, may be very strong. One has to be smart in order to recognise smart behaviour, so preference and preferred feature are strongly connected. But that's only my opinion.

Boogert et al., 2011 1 reviews the current knowledge about animal preferences for cognition skills. They conclude that there is very little data on this subject. The given examples are:

1) Preference for elaborating birds songs (as songs are not inborn and have to be learned)

2) Spatial abilities:

In meadow voles (Microtus pennsylvanicus), males with better spatial learning and memory abilities were not only found to have larger home ranges and to locate more females in the field (Spritzer, Solomon, et al. 2005 2) but were also preferred by females in mate-choice tests, even though the females did not observe males' performance on spatial tests (Spritzer, Meikle, et al. 2005 3).

In guppies (Poecilia reticulata), males that learned faster to swim through mazes to gain a food reward were found to be more attractive to females (Shohet and Watt 2009 4). However, females were not able to see the males' performance in the mazes. Although male learning ability was weakly correlated with saturation of the orange patches on his body (a sexually selected trait (… )), orange saturation surprisingly did not correlate with female preferences. Thus, the cues leading female guppies to prefer faster learners are unknown.

It is possible, that females base their choose on some factors that correlates with cognitive skills or on total wellness, what may depend on intelligence.

3) bowerbird's abilities to build bowers (courtship constructions):

Comparative studies across bowerbird species have shown that relative brain size is larger in species that build bowers than in closely related nonbuilding species (Madden 2001 5). In addition, relative brain size increases with the species-typical complexity of the bower (Madden 2001 5), and a comparative study on the relative size of specific brain regions showed that species with more complex bowers have a relatively larger cerebellum (Day et al. 2005 6).

4) foraging performance

A recent experiment by Snowberg and Benkman (2009) 7 using red crossbills (Loxia curvirostra) showed that, after observing 2 males extracting seeds from conifer cones, females associated preferentially with the more efficient forager of the 2. The authors were able to exclude female choice for correlated traits by experimentally manipulating foraging efficiency, such that fewer seeds were available in the cones of one of the males. The males were also swapped between treatments (i.e., slow vs. fast forager) so that male identity could not explain the females' preferences for the most efficient forager.


Another way that intelligence may be favored by sexual selection is "cheating" during courtship. For example most frog species call to attract females. But this signal may also attract aggresive rivals or predators. Some males, especially the weaker ones, do not call but stay near calling individual. This allows them to avoid confrontation and wait for approaching females [8]. The successfulness of this strategy may depend on how "smart" the individual is (only my opinion).

[1] Boogert, N. J., Fawcett, T. W., & Lefebvre, L. (2011). Mate choice for cognitive traits: a review of the evidence in nonhuman vertebrates. Behavioral Ecology, 22(3), 447-459.

[2] Spritzer MD, Solomon NG, Meikle DB. 2005. Influence of scramble competition for mates upon the spatial ability of male meadow voles. Anim Behav. 69:375-386.

[3] Spritzer MD, Meikle DB, Solomon NG. 2005. Female choice based on male spatial ability and aggressiveness among meadow voles. Anim Behav. 69:1121-1130.

[4] Shohet AJ, Watt PJ. 2009. Female guppies Poecilia reticulata prefer males that can learn fast. J Fish Biol. 75:1323-1330.

[5] Madden J. 2001. Sex, bowers and brains. Proc R Soc Lond B Biol Sci. 268:833-838.

[6] Day LB, Westcott DA, Olster DH. 2005. Evolution of bower complexity and cerebellum size in bowerbirds. Brain Behav Evol. 66:62-72

[7] Snowberg LK, Benkman CW. 2009. Mate choice based on a key ecological performance trait. J Evol Biol. 22:762-769.

[8] Bateson P. 1985. Mate choice. Cambridge University Press. 181-210


I know nothing about biology however I did watch an amazing PBS documentary on cuttlefish that I think is fairly relevent.

From http://www.pbs.org/wgbh/nova/nature/kings-of-camouflage.html

NARRATOR: During mating, males outnumber the females, sometimes 10 to one. And they're all looking for the chance to pass on their genes. While a female lays eggs beneath a rock, a big male tries to monopolize her, staving off the other hopeful suitors.

Sometimes intimidation alone won't work, and the competitors hurl themselves into a violent and bizarre looking wrestling match.

Like an octopus, they'll squirt out an inky smokescreen when it's time for a hasty retreat.

But size and strength aren't the only ways to impress the ladies.

Thanks to the cuttlefish's skin morphing talents, the smaller males have a clever trick up their sleeve.

MARK NORMAN: The really interesting thing in this system is actually far less obvious, and when you first dive with them, you don't see it. It takes a while before you realize what's going on.

The small males, who have no chance in a contest with a big male, are actually doing something completely different. They're effectively cross-dressing. They're dressing up as a female, by pulling in their webs and putting on this mottled color pattern and gliding past these big, aggressive male, pretending to be a female, and will come in to the female underneath.

And what happens is, as another big male comes in and a potential conflict between these big guys starts up, the sneaker males start mating with her, successfully mate with the female, while the big guy isn't even aware of it.

NARRATOR: The cross-dressers' success is all the more impressive because the females often play hard to get, as Roger Hanlon has seen firsthand.

ROGER HANLON: These females are very picky. They reject 70 percent of approaches for mating. Yet they only reject 30 percent of the cross-dressing males. So this trick gets them in the door, so to speak, past the fighting male, and they're accepted by the female.


Social construction of gender

The social construction of gender is a theory in feminism and sociology about the manifestation of cultural origins, mechanisms, and corollaries of gender perception and expression in the context of interpersonal and group social interaction. Specifically, the social construction of gender stipulates that gender roles are an achieved "status" in a social environment, which implicitly and explicitly categorize people and therefore motivate social behaviors. [1]

A related matter in feminist theory is the relationship between the ascribed status of assigned sex (male or female) and their achieved status counterparts in gender (masculine and feminine).


Mate Choice Copying in Humans

There is substantial evidence that in human mate choice, females directly select males based on male display of both physical and behavioral traits. In non-humans, there is additionally a growing literature on indirect mate choice, such as choice through observing and subsequently copying the mating preferences of conspecifics (mate choice copying). Given that humans are a social species with a high degree of sharing information, long-term pair bonds, and high parental care, it is likely that human females could avoid substantial costs associated with directly searching for information about potential males by mate choice copying. The present study was a test of whether women perceived men to be more attractive when men were presented with a female date or consort than when they were presented alone, and whether the physical attractiveness of the female consort affected women’s copying decisions. The results suggested that women’s mate choice decision rule is to copy only if a man’s female consort is physically attractive. Further analyses implied that copying may be a conditional female mating tactic aimed at solving the problem of informational constraints on assessing male suitability for long-term sexual relationships, and that lack of mate choice experience, measured as reported lifetime number of sex partners, is also an important determinant of copying.

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Contents

In sociobiology and behavioural ecology, the term "mating system" is used to describe the ways in which animal societies are structured in relation to sexual behaviour. The mating system specifies which males mate with which females, and under what circumstances. There are four basic systems:

The four basic mating systems [4] : 160–161 [5]
Single female Multiple females
Single male Monogamy Polygyny
Multiple males Polyandry Polygynandry

Monogamy Edit

Monogamy occurs when one male mates with one female exclusively. A monogamous mating system is one in which individuals form long-lasting pairs and cooperate in raising offspring. These pairs may last for a lifetime, such as in pigeons, [6] or it may occasionally change from one mating season to another, such as in emperor penguins. [7] In contrast with tournament species, these pair-bonding species have lower levels of male aggression, competition and little sexual dimorphism. Zoologists and biologists now have evidence that monogamous pairs of animals are not always sexually exclusive. Many animals that form pairs to mate and raise offspring regularly engage in sexual activities with extra-pair partners. [8] [9] [10] [11] This includes previous examples, such as swans. Sometimes, these extra-pair sexual activities lead to offspring. Genetic tests frequently show that some of the offspring raised by a monogamous pair come from the female mating with an extra-pair male partner. [9] [12] [13] [14] These discoveries have led biologists to adopt new ways of talking about monogamy. According to Ulrich Reichard (2003):

Social monogamy refers to a male and female's social living arrangement (e.g., shared use of a territory, behaviour indicative of a social pair, and/or proximity between a male and female) without inferring any sexual interactions or reproductive patterns. In humans, social monogamy takes the form of monogamous marriage. Sexual monogamy is defined as an exclusive sexual relationship between a female and a male based on observations of sexual interactions. Finally, the term genetic monogamy is used when DNA analyses can confirm that a female-male pair reproduce exclusively with each other. A combination of terms indicates examples where levels of relationships coincide, e.g., sociosexual and sociogenetic monogamy describe corresponding social and sexual, and social and genetic monogamous relationships, respectively. [15]

Whatever makes a pair of animals socially monogamous does not necessarily make them sexually or genetically monogamous. Social monogamy, sexual monogamy, and genetic monogamy can occur in different combinations.

Social monogamy is relatively rare in the animal kingdom. The actual incidence of social monogamy varies greatly across different branches of the evolutionary tree. Over 90% of avian species are socially monogamous. [10] [16] This stands in contrast to mammals. Only 3% of mammalian species are socially monogamous, although up to 15% of primate species are. [10] [16] Social monogamy has also been observed in reptiles, fish, and insects.

Sexual monogamy is also rare among animals. Many socially monogamous species engage in extra-pair copulations, making them sexually non-monogamous. For example, while over 90% of birds are socially monogamous, "on average, 30% or more of the baby birds in any nest [are] sired by someone other than the resident male." [17] Patricia Adair Gowaty has estimated that, out of 180 different species of socially monogamous songbirds, only 10% are sexually monogamous. [18]

The incidence of genetic monogamy, determined by DNA fingerprinting, varies widely across species. For a few rare species, the incidence of genetic monogamy is 100%, with all offspring genetically related to the socially monogamous pair. But genetic monogamy is strikingly low in other species. Barash and Lipton note:

The highest known frequency of extra-pair copulations are found among the fairy-wrens, lovely tropical creatures technically known as Malurus splendens and Malurus cyaneus. More than 65% of all fairy-wren chicks are fathered by males outside the supposed breeding group. [16] p. 12

Such low levels of genetic monogamy have surprised biologists and zoologists, forcing them to rethink the role of social monogamy in evolution. They can no longer assume social monogamy determines how genes are distributed in a species. The lower the rates of genetic monogamy among socially monogamous pairs, the less of a role social monogamy plays in determining how genes are distributed among offspring.

Polygamy Edit

The term polygamy is an umbrella term used to refer generally to non-monogamous matings. As such, polygamous relationships can be polygynous, polyandrous or polygynandrous. In a small number of species, individuals can display either polygamous or monogamous behaviour depending on environmental conditions. An example is the social wasp Apoica flavissima. [ citation needed ] In some species, polygyny and polyandry is displayed by both sexes in the population. Polygamy in both sexes has been observed in red flour beetle (Tribolium castaneum). Polygamy is also seen in many Lepidoptera species including Mythimna unipuncta (true armyworm moth). [19]

A tournament species is one in which "mating tends to be highly polygamous and involves high levels of male-male aggression and competition." [20] Tournament behaviour often correlates with high levels of sexual dimorphism, examples of species including chimpanzees and baboons. Most polygamous species present high levels of tournament behaviour, with a notable exception being bonobos. [ citation needed ]

Polygyny Edit

Polygyny occurs when one male gets exclusive mating rights with multiple females. In some species, notably those with harem-like structures, only one of a few males in a group of females will mate. Technically, polygyny in sociobiology and zoology is defined as a system in which a male has a relationship with more than one female, but the females are predominantly bonded to a single male. Should the active male be driven out, killed, or otherwise removed from the group, in a number of species the new male will ensure that breeding resources are not wasted on another male's young. [21] The new male may achieve this in many different ways, including:

  • competitive infanticide: in lions, hippopotamuses, and some monkeys, the new male will kill the offspring of the previous alpha male to cause their mothers to become receptive to his sexual advances since they are no longer nursing. To prevent this, many female primates exhibit ovulation cues among all males, and show situation-dependent receptivity. [22] to miscarriage: amongst wild horses and baboons, the male will "systematically harass" pregnant females until they miscarry. -based spontaneous abortion
  • in some rodents such as mice, a new male with a different scent will cause females who are pregnant to spontaneously fail to implant recently fertilised eggs. This does not require contact it is mediated by scent alone. It is known as the Bruce effect.

Von Haartman specifically described the mating behaviour of the European pied flycatcher as successive polygyny. [23] Within this system, the males leave their home territory once their primary female lays her first egg. Males then create a second territory, presumably in order to attract a secondary female to breed. Even when they succeed at acquiring a second mate, the males typically return to the first female to exclusively provide for her and her offspring. [24]

Polygynous mating structures are estimated to occur in up to 90% of mammal species. [25] As polygyny is the most common form of polygamy among vertebrates (including humans, to some extent), it has been studied far more extensively than polyandry or polygynandry.

Polyandry Edit

Polyandry occurs when one female gets exclusive mating rights with multiple males. In some species, such as redlip blennies, both polygyny and polyandry are observed. [26]

The males in some deep sea anglerfishes are much smaller than the females. When they find a female they bite into her skin, releasing an enzyme that digests the skin of their mouth and her body and fusing the pair down to the blood-vessel level. The male then slowly atrophies, losing first his digestive organs, then his brain, heart, and eyes, ending as nothing more than a pair of gonads, which release sperm in response to hormones in the female's bloodstream indicating egg release. This extreme sexual dimorphism ensures that, when the female is ready to spawn, she has a mate immediately available. [27] A single anglerfish female can "mate" with many males in this manner.

Polygynandry Edit

Polygynandry occurs when multiple males mate indiscriminately with multiple females. The numbers of males and females need not be equal, and in vertebrate species studied so far, there are usually fewer males. Two examples of systems in primates are promiscuous mating chimpanzees and bonobos. These species live in social groups consisting of several males and several females. Each female copulates with many males, and vice versa. In bonobos, the amount of promiscuity is particularly striking because bonobos use sex to alleviate social conflict as well as to reproduce. [28] This mutual promiscuity is the approach most commonly used by spawning animals, and is perhaps the "original fish mating system." [4] : 161 Common examples are forage fish, such as herrings, which form huge mating shoals in shallow water. The water becomes milky with sperm and the bottom is draped with millions of fertilised eggs. [4] : 161

Female and male sexual behaviour differ in many species. Often, males are more active in initiating mating, and bear the more conspicuous sexual ornamentation like antlers and colourful plumage. This is a result of anisogamy, where sperm are smaller and much less costly (energetically) to produce than eggs. This difference in physiological cost means that males are more limited by the number of mates they can secure, while females are limited by the quality of genes of her mates, a phenomenon known as Bateman's principle. [29] Many females also have extra reproductive burdens in that parental care often falls mainly, or exclusively, on them. Thus, females are more limited in their potential reproductive success. [30] In species where males take on more of the reproductive costs, such as sea horses and jacanas, the role is reversed, and the females are larger, more aggressive and more brightly coloured than the males.

In hermaphroditic animals, the costs of parental care can be evenly distributed between the sexes, e.g. earthworms. In some species of planarians, sexual behaviour takes the form of penis fencing. In this form of copulation, the individual that first penetrates the other with the penis, forces the other to be female, thus carrying the majority of the cost of reproduction. [31] Post mating, banana slugs will some times gnaw off their partners penis as an act of sperm competition called apophallation. [32] This is costly as they must heal, and spend more energy courting conspecifics that can act as male and female. A hypothesis suggests these slugs may be able to compensate the loss of the male function by directing energy that would have been put towards it to the female function. [33] In the grey slug, the sharing of cost leads to a spectacular display, where the mates suspend themselves high above the ground from a slime thread, ensuring none of them can refrain from taking on the cost of egg-bearer. [34]

Many animal species have specific mating (or breeding) periods e.g. (seasonal breeding) so that offspring are born or hatch at an optimal time. In marine species with limited mobility and external fertilisation like corals, sea urchins and clams, the timing of the common spawning is the only externally visible form of sexual behaviour. In areas with continuously high primary production, some species have a series of breeding seasons throughout the year. This is the case with most primates (who are primarily tropical and subtropical animals). Some animals (opportunistic breeders) breed dependent upon other conditions in their environment aside from time of year.

Mammals Edit

Mating seasons are often associated with changes to herd or group structure, and behavioural changes, including territorialism amongst individuals. These may be annual (e.g. wolves), biannual (e.g. dogs) or more frequently (e.g. horses). During these periods, females of most mammalian species are more mentally and physically receptive to sexual advances, a period scientifically described as oestrus but commonly described as being "in season" or "in heat". Sexual behaviour may occur outside oestrus, [35] and such acts as do occur are not necessarily harmful. [36]

Some mammals (e.g. domestic cats, rabbits and camelids) are termed "induced ovulators". For these species, the female ovulates due to an external stimulus during, or just prior, to mating, rather than ovulating cyclically or spontaneously. Stimuli causing induced ovulation include the sexual behaviour of coitus, sperm and pheromones. Domestic cats have penile spines. Upon withdrawal of a cat's penis, the spines rake the walls of the female's vagina, which may cause ovulation. [37] [38]

Amphibians Edit

For many amphibians, an annual breeding cycle applies, typically regulated by ambient temperature, precipitation, availability of surface water and food supply. This breeding season is accentuated in temperate regions, in boreal climate the breeding season is typically concentrated to a few short days in the spring. Some species, such as the Rana clamitans (green frog), spend from June to August defending their territory. In order to protect these territories, they use five vocalizations. [39]

Fish Edit

Like many coral reef dwellers, the clownfish spawn around the time of the full moon in the wild. In a group of clownfish, there is a strict dominance hierarchy. The largest and most aggressive female is found at the top. Only two clownfish, a male and a female, in a group reproduce through external fertilisation. Clownfish are sequential hermaphrodites, meaning that they develop into males first, and when they mature, they become females. If the female clownfish is removed from the group, such as by death, one of the largest and most dominant males will become a female. The remaining males will move up a rank in the hierarchy.

Various neurohormones stimulate sexual wanting in animals. In general, studies have suggested that dopamine is involved in sexual incentive motivation, oxytocin and melanocortins in sexual attraction, and noradrenaline in sexual arousal. [40] Vasopressin is also involved in the sexual behaviour of some animals. [41]

Neurohormones in the mating systems of voles Edit

The mating system of prairie voles is monogamous after mating, they form a lifelong bond. In contrast, montane voles have a polygamous mating system. When montane voles mate, they form no strong attachments, and separate after copulation. Studies [ citation needed ] on the brains of these two species have found that it is two neurohormones and their respective receptors that are responsible for these differences in mating strategies. Male prairie voles release vasopressin after copulation with a partner, and an attachment to their partner then develops. Female prairie voles release oxytocin after copulation with a partner, and similarly develop an attachment to their partner.

Neither male nor female montane voles release high quantities of oxytocin or vasopressin when they mate. Even when injected with these neurohormones, their mating system does not change. In contrast, if prairie voles are injected with the neurohormones, they may form a lifelong attachment, even if they have not mated. It's believed [ by whom? ] that the differing response to the neurohormones between the two species is due to a difference in the number of oxytocin and vasopressin receptors. Prairie voles have a greater number of oxytocin and vasopressin receptors compared to montane voles, and are therefore more sensitive to those two neurohormones. It's believed that it's the quantity of receptors, rather than the quantity of the hormones, that determines the mating system and bond-formation of either species.

Oxytocin and rat sexual behaviour Edit

Mother rats experience a postpartum estrus which makes them highly motivated to mate. However, they also have a strong motivation to protect their newly born pups. As a consequence, the mother rat solicits males to the nest but simultaneously becomes aggressive towards them to protect her young. If the mother rat is given injections of an oxytocin receptor antagonist, they no longer experience these maternal motivations. [42]

Prolactin influences social bonding in rats. [42]

Oxytocin and primate sexual behaviour Edit

Oxytocin plays a similar role in non-human primates as it does in humans.

Grooming, sex, and cuddling frequencies correlate positively with levels of oxytocin. As the level of oxytocin increases so does sexual motivation. While oxytocin plays a major role in parent child relationships, it is also found to play a role in adult sexual relationships. Its secretion affects the nature of the relationship or if there will even be a relationship at all. [ citation needed ] [43]

Studies have shown that oxytocin is higher in monkeys in lifelong monogamous relationships compared to monkeys which are single. Furthermore, the oxytocin levels of the couples correlate positively when the oxytocin secretion of one increases the other one also increases. Higher levels of oxytocin are related to monkeys expressing more behaviours such as cuddling, grooming and sex, while lower levels of oxytocin reduce motivation for these activities. [ citation needed ]

Research on oxytocin's role in the animal brain suggests that it plays less of a role in behaviours of love and affection than previously believed. "When oxytocin was first discovered in 1909, it was thought mostly to influence a mother's labour contractions and milk let-down. Then, in the 1990s, research with prairie voles found that giving them a dose of oxytocin resulted in the formation of a bond with their future mate (Azar, 40)." Oxytocin has since been treated by the media as the sole player in the "love and mating game" in mammals. This view, however, is proving to be false as, "most hormones don't influence behaviour directly. Rather, they affect thinking and emotions in variable ways (Azar, 40)." There is much more involved in sexual behaviour in the mammalian animal than oxytocin and vasopressin can explain. [44] [45] [46] [47] [48] [49] [50]

Pleasure Edit

It is often assumed that animals do not have sex for pleasure, or alternatively that humans, pigs, bonobos (and perhaps dolphins and one or two more species of primates) are the only species that do. This is sometimes stated as "animals mate only for reproduction". This view is considered a misconception by some scholars. [51] [52] Jonathan Balcombe argues that the prevalence of non-reproductive sexual behaviour in certain species suggests that sexual stimulation is pleasurable. He also points to the presence of the clitoris in some female mammals, and evidence for female orgasm in primates. [53] On the other hand, it is impossible to know the subjective feelings of animals, [40] and the notion that non-human animals experience emotions similar to humans is a contentious subject. [54] [55] [56] [57]

A 2006 Danish Animal Ethics Council report, [58] which examined current knowledge of animal sexuality in the context of legal queries concerning sexual acts by humans, has the following comments, primarily related to domestically common animals:

Even though the evolution-related purpose of mating can be said to be reproduction, it is not actually the creating of offspring which originally causes them to mate. It is probable that they mate because they are motivated for the actual copulation, and because this is connected with a positive experience. It is therefore reasonable to assume that there is some form of pleasure or satisfaction connected with the act. This assumption is confirmed by the behaviour of males, who in the case of many species are prepared to work to get access to female animals, especially if the female animal is in oestrus, and males who for breeding purposes are used to having sperm collected become very eager, when the equipment they associate with the collection is taken out. . . . There is nothing in female mammals' anatomy or physiology that contradicts that stimulation of the sexual organs and mating is able to be a positive experience. For instance, the clitoris acts in the same way as with women, and scientific studies have shown that the success of reproduction is improved by stimulation of clitoris on (among other species) cows and mares in connection with insemination, because it improves the transportation of the sperm due to contractions of the inner genitalia. This probably also applies to female animals of other animal species, and contractions in the inner genitals are seen e.g. also during orgasm for women. It is therefore reasonable to assume that sexual intercourse may be linked with a positive experience for female animals.

Koinophilia is the love of the "normal" or phenotypically common (from the Greek κοινός , koinós, meaning "usual" or "common"). [59] The term was introduced to scientific literature in 1990, and refers to the tendency of animals seeking a mate to prefer that mate not to have any unusual, peculiar or deviant features. [59] Similarly, animals preferentially choose mates with low fluctuating asymmetry. [60] However, animal sexual ornaments can evolve through runaway selection, which is driven by (usually female) selection for non-standard traits. [61]

The field of study of sexuality in non-human species was a long-standing taboo. [62] In the past, researchers sometimes failed to observe, miscategorised or misdescribed sexual behaviour which did not meet their preconceptions—their bias tended to support what would now be described as conservative sexual mores. An example of overlooking behaviour relates to descriptions of giraffe mating:

When nine out of ten pairings occur between males, "[e]very male that sniffed a female was reported as sex, while anal intercourse with orgasm between males was only [categorized as] 'revolving around' dominance, competition or greetings." [62]

In the 21st century, liberal social or sexual views are often projected upon animal subjects of research. Popular discussions of bonobos are a frequently cited example. Current research frequently expresses views such as that of the Natural History Museum at the University of Oslo, which in 2006 held an exhibition on animal sexuality:

Many researchers have described homosexuality as something altogether different from sex. They must realise that animals can have sex with who they will, when they will and without consideration to a researcher's ethical principles. [62]

Other animal activities may be misinterpreted due to the frequency and context in which animals perform the behaviour. For example, domestic ruminants display behaviours such as mounting and head-butting. This often occurs when the animals are establishing dominance relationships and are not necessarily sexually motivated. Careful analysis must be made to interpret what animal motivations are being expressed by those behaviours. [63]

Reproductive sexual behaviour Edit

Copulation Edit

Copulation is the union of the male and female sex organs, the sexual activity specifically organized to transmit male sperm into the body of the female. [64]

Cuckoldry Edit

Alternative male strategies which allow small males to engage in cuckoldry can develop in species such as fish where spawning is dominated by large and aggressive males. Cuckoldry is a variant of polyandry, and can occur with sneak spawners. A sneak spawner is a male that rushes in to join the spawning rush of a spawning pair. [65] A spawning rush occurs when a fish makes a burst of speed, usually on a near vertical incline, releasing gametes at the apex, followed by a rapid return to the lake or sea floor or fish aggregation. [66] Sneaking males do not take part in courtship. In salmon and trout, for example, jack males are common. These are small silvery males that migrate upstream along with the standard, large, hook-nosed males and that spawn by sneaking into redds to release sperm simultaneously with a mated pair. This behaviour is an evolutionarily stable strategy for reproduction, because it is favoured by natural selection just like the "standard" strategy of large males. [67]

Hermaphroditism Edit

Hermaphroditism occurs when a given individual in a species possesses both male and female reproductive organs, or can alternate between possessing first one, and then the other. Hermaphroditism is common in invertebrates but rare in vertebrates. It can be contrasted with gonochorism, where each individual in a species is either male or female, and remains that way throughout their lives. Most fish are gonochorists, but hermaphroditism is known to occur in 14 families of teleost fishes. [68]

Usually hermaphrodites are sequential, meaning they can switch sex, usually from female to male (protogyny). This can happen if a dominant male is removed from a group of females. The largest female in the harem can switch sex over a few days and replace the dominant male. [68] This is found amongst coral reef fishes such as groupers, parrotfishes and wrasses. As an example, most wrasses are protogynous hermaphrodites within a haremic mating system. [69] [70] It is less common for a male to switch to a female (protandry). [4] : 162 A common example of a protandrous species are clownfish—if the larger, dominant female dies, in many cases, the reproductive male gains weight and becomes the female. [71] [72] Hermaphroditism allows for complex mating systems. Wrasses exhibit three different mating systems: polygynous, lek-like, and promiscuous mating systems. [73]

Sexual cannibalism Edit

Sexual cannibalism is a behaviour in which a female animal kills and consumes the male before, during, or after copulation. Sexual cannibalism confers fitness advantages to both the male and female. [74] Sexual cannibalism is common among insects, arachnids [75] and amphipods. [75] There is also evidence of sexual cannibalism in gastropods and copepods. [76]

Sexual coercion Edit

Sex in a forceful or apparently coercive context has been documented in a variety of species. In some herbivorous herd species, or species where males and females are very different in size, the male dominates sexually by force and size. [ citation needed ]

Some species of birds have been observed combining sexual intercourse with apparent violent assault these include ducks, [77] [78] and geese. [79] Female white-fronted bee-eaters are subjected to forced copulations. When females emerge from their nest burrows, males sometimes force them to the ground and mate with them. Such forced copulations are made preferentially on females who are laying and who may therefore lay eggs fertilized by the male. [80]

It has been reported that young male elephants in South Africa sexually coerced and killed rhinoceroses. [81] This interpretation of the elephants' behaviour was disputed by one of the original study's authors, who said there was "nothing sexual about these attacks". [82]

Parthenogenesis Edit

Parthenogenesis is a form of asexual reproduction in which growth and development of embryos occur without fertilisation. [83] Technically, parthenogenesis is not a behaviour, however, sexual behaviours may be involved.

Whip-tailed lizard females have the ability to reproduce through parthenogenesis and as such males are rare and sexual breeding non-standard. Females engage in "pseudocopulation" [84] to stimulate ovulation, with their behaviour following their hormonal cycles during low levels of oestrogen, these (female) lizards engage in "masculine" sexual roles. Those animals with currently high oestrogen levels assume "feminine" sexual roles. Lizards that perform the courtship ritual have greater fecundity than those kept in isolation due to an increase in hormones triggered by the sexual behaviours. So, even though asexual whiptail lizards populations lack males, sexual stimuli still increase reproductive success. From an evolutionary standpoint these females are passing their full genetic code to all of their offspring rather than the 50% of genes that would be passed in sexual reproduction. [ citation needed ]

It is rare to find true parthenogenesis in fishes, where females produce female offspring with no input from males. All-female species include the Texas silverside, Menidia clarkhubbsi [85] and a complex of Mexican mollies. [4] : 162

Parthenogenesis has been recorded in 70 vertebrate species [86] including hammerhead sharks, [87] blacktip sharks, [88] amphibians [89] and lizards. [90]

Unisexuality Edit

Unisexuality occurs when a species is all-male or all-female. Unisexuality occurs in some fish species and can take complex forms. Squalius alburnoides, a minnow found in several river basins in Portugal and Spain, appears to be an all-male species. The existence of this species illustrates the potential complexity of mating systems in fish. The species originated as a hybrid between two species and is diploid but not hermaphroditic. It can have triploid and tetraploid forms, including all-female forms that reproduce mainly through hybridogenesis. [91]

Others Edit

  • Interbreeding: Hybrid offspring can result from the mating of two organisms of distinct but closely related parent species, although the resulting offspring is not always fertile. According to Alfred Kinsey, genetic studies on wild animal populations have shown a "large number" of inter-species hybrids. [92]
  • Prostitution: There are reports that animals occasionally engage in prostitution. A small number of pair-bonded females within a group of penguins took nesting material (stones) after copulating with a non-partner male. The researcher stated "I was watching opportunistically, so I can't give an exact figure of how common it really is." [93] It has been reported that "bartering of meat for sex . forms part of the social fabric of a troop of wild chimps living in the Tai National Park in the Côte d’Ivoire." [94]
  • Pavlovian conditioning: The sexualisation of objects or locations is recognised in the animal breeding world. For example, male animals may become sexually aroused upon visiting a location where they have been allowed to have sex before, or upon seeing a stimulus previously associated with sexual activity such as an artificial vagina. [95] Sexual preferences for certain cues can be artificially induced in rats by pairing scents or objects with their early sexual experiences. [96] The primary motivation of this behaviour is Pavlovian conditioning, and the association is due to a conditioned response (or association) formed with a distinctive "reward". [96]
  • Viewing images: A study using four adult male rhesus macaques (Macaca mulatta) showed that male rhesus macaques will give up a highly valued item, juice, to see images of the faces or perineum of high-status females. [97] Encouraging captive pandas to mate is problematic. Showing young male pandas "panda pornography" is credited with a recent population boom among pandas in captivity in China. One researcher attributed the success to the sounds on the recordings. [98]
  • Copulatory wounding and Traumatic Insemination: Injury to a partner's genital tract during mating occurs in at least 40 taxa, ranging from fruit flies to humans. However, it often goes unnoticed due to its cryptic nature and because of internal wounds not visible outside. [99]

Non-reproductive sexual behaviour Edit

There is a range of behaviours that animals perform that appear to be sexually motivated but which can not result in reproduction. These include:

    : Some species, both male and female, masturbate, both when partners are available and otherwise. [100][101] : Several species engage in both autofellatio and oral sex. This has been documented in brown bears, [102]Tibetan macaques, [103]wolves, [104]goats, primates, bats, [105][106]cape ground squirrels[107] and sheep. In the greater short-nosed fruit bat, copulation by males is dorsoventral and the females lick the shaft or the base of the male's penis, but not the glans which has already penetrated the vagina. While the females do this, the penis is not withdrawn and research has shown a positive relationship between length of the time that the penis is licked and the duration of copulation. Post copulation genital grooming has also been observed. [108] : Same-sex sexual behaviour occurs in a range of species, especially in social species, particularly in marine birds and mammals, monkeys, and the great apes. As of 1999 [update] , the scientific literature contained reports of homosexual behaviour in at least 471 wild species. [109] Organisers of the Against Nature? exhibit stated that "homosexuality has been observed among 1,500 species, and that in 500 of those it is well documented." [110]
    : This is sexual activity in which one animal rubs his or her genitals against the genitals of another animal. This is stated to be the "bonobo's most typical sexual pattern, undocumented in any other primate". [112][113] : Some animals opportunistically mate with individuals of another species. [114] : Male stoats (Mustela erminea) will sometimes mate with infant females of their species. [115] This is a natural part of their reproductive biology—they have a delayed gestation period, so these females give birth the following year when they are fully grown. Juvenile male chimpanzees have been recorded mounting and copulating with immature chimps. Infants in bonobo societies are often involved in sexual behaviour. [116] : This describes when an animal engages in a sexual act with a dead animal. It has been observed in mammals, birds, reptiles and frogs. [117] : This describes when an animal shows sexual behaviour towards both males and females. : This is when females mate with males outside of their conceptive period. [118][22]

Seahorse Edit

Seahorses, once considered to be monogamous species with pairs mating for life, were described in a 2007 study as "promiscuous, flighty, and more than a little bit gay". [119] Scientists at 15 aquaria studied 90 seahorses of three species. Of 3,168 sexual encounters, 37% were same-sex acts. Flirting was common (up to 25 potential partners a day of both sexes) only one species (the British spiny seahorse) included faithful representatives, and for these 5 of 17 were faithful, 12 were not. Bisexual behaviour was widespread and considered "both a great surprise and a shock", with big-bellied seahorses of both sexes not showing partner preference. 1,986 contacts were male-female, 836 were female-female and 346 were male-male. [119]

Bonobo Edit

Among bonobos, males and females engage in sexual behaviour with the same and the opposite sex, with females being particularly noted for engaging in sexual behaviour with each other and at up to 75% of sexual activity being non-reproductive, as being sexually active does not necessarily correlate with their ovulation cycles. [112] Sexual activity occurs between almost all ages and sexes of bonobo societies. [120] [121] Primatologist Frans de Waal believes that bonobos use sexual activity to resolve conflict between individuals. [28] [122] Immature bonobos, contrariwise, perform genital contact when relaxed. [121]

Similar same-sex sexual behaviours occur in both male and female macaques. [123] It is thought to be done for pleasure as an erect male mounts and thrusts upon or into another male. [123] [124] Sexual receptivity can also be indicated by red faces and shrieking. [123] Mutual ejaculation after a combination of anal intercourse and masturbation has also been witnessed, although it may be rare. [124] In comparison to socio-sexual behaviours such as dominance displays, homosexual mounts last longer, happen in series, and usually involve pelvic thrusting. [123]

Females are also thought to participate for pleasure as vulvar, perineal, and anal stimulation is part of these interactions. The stimulation can come from their own tails, mounting their partner, thrusting or a combination of these. [125]

Dolphin Edit

Male bottlenose dolphins have been observed working in pairs to follow or restrict the movement of a female for weeks at a time, waiting for her to become sexually receptive. The same pairs have also been observed engaging in intense sexual play with each other. Janet Mann, a professor of biology and psychology at Georgetown University, argues [126] that the common same-sex behaviour among male dolphin calves is about bond formation and benefits the species evolutionarily. They cite studies that have shown the dolphins later in life are bisexual and the male bonds forged from homosexuality work for protection as well as locating females with which to reproduce. In 1991, an English man was prosecuted for allegedly having sexual contact with a dolphin. [127] The man was found not guilty after it was revealed at trial that the dolphin was known to tow bathers through the water by hooking his penis around them. [127]

Hyena Edit

The female spotted hyena has a unique urinary-genital system, closely resembling the penis of the male, called a pseudo-penis. Dominance relationships with strong sexual elements are routinely observed between related females. They are notable for using visible sexual arousal as a sign of submission but not dominance in males as well as females (females have a sizeable erectile clitoris). [128] It is speculated that to facilitate this, their sympathetic and parasympathetic nervous systems may be partially reversed in respect to their reproductive organs. [129]

Vertebrates Edit

Mammals Edit

Mammals mate by vaginal copulation. To achieve this, the male usually mounts the female from behind. [130] The female may exhibit lordosis in which she arches her back ventrally to facilitate entry of the penis. Amongst the land mammals, other than humans, only bonobos mate in a face-to-face position, [131] [ better source needed ] as the females' anatomy seems to reflect, [112] although ventro-ventral copulation has also been observed in Rhabdomys. [132] Some sea mammals copulate in a belly-to-belly position. [133] [134] Some camelids mate in a lying-down position. [135] In most mammals ejaculation occurs after multiple intromissions, [136] but in most primates, copulation consists of one brief intromission. [137] In most ruminant species, a single pelvic thrust occurs during copulation. [138] [139] In most deer species, a copulatory jump also occurs. [140] [141]

During mating, a "copulatory tie" occurs in mammals such as fossas, [142] canids [143] and Japanese martens. [144] A "copulatory lock" also occurs in some primate species, such as Galago senegalensis. [145]

The copulatory behaviour of many mammalian species is affected by sperm competition. [146]

Some females have concealed fertility, making it difficult for males to evaluate if a female is fertile. This is costly as ejaculation expends much energy. [22]

Invertebrates Edit

Invertebrates are often hermaphrodites. Some hermaphroditic land snails begin mating with an elaborate tactile courting ritual. The two snails circle around each other for up to six hours, touching with their tentacles, and biting lips and the area of the genital pore, which shows some preliminary signs of the eversion of the penis. As the snails approach mating, hydraulic pressure builds up in the blood sinus surrounding an organ housing a sharpened dart. The dart is made of calcium carbonate or chitin, and is called a love dart. Each snail manoeuvres to get its genital pore in the best position, close to the other snail's body. Then, when the body of one snail touches the other snail's genital pore, it triggers the firing of the love dart. [147] After the snails have fired their darts, they copulate and exchange sperm as a separate part of the mating progression. The love darts are covered with a mucus that contains a hormone-like substance that facilitates the survival of the sperm. [148] [149]

Penis fencing is a mating behaviour engaged in by certain species of flatworm, such as Pseudobiceros bedfordi. Species which engage in the practice are hermaphroditic, possessing both eggs and sperm-producing testes. [150] The species "fence" using two-headed dagger-like penises which are pointed, and white in colour. One organism inseminates the other. The sperm is absorbed through pores in the skin, causing fertilisation.

Corals can be both gonochoristic (unisexual) and hermaphroditic, each of which can reproduce sexually and asexually. Reproduction also allows corals to settle new areas. Corals predominantly reproduce sexually. 25% of hermatypic corals (stony corals) form single sex (gonochoristic) colonies, while the rest are hermaphroditic. [151] About 75% of all hermatypic corals "broadcast spawn" by releasing gametes – eggs and sperm – into the water to spread offspring. The gametes fuse during fertilisation to form a microscopic larva called a planula, typically pink and elliptical in shape. [152] Synchronous spawning is very typical on the coral reef and often, even when multiple species are present, all corals spawn on the same night. This synchrony is essential so that male and female gametes can meet. Corals must rely on environmental cues, varying from species to species, to determine the proper time to release gametes into the water. The cues involve lunar changes, sunset time, and possibly chemical signalling. [151] Synchronous spawning may form hybrids and is perhaps involved in coral speciation. [153]

Butterflies spend much time searching for mates. When the male spots a mate, he will fly closer and release pheromones. He then performs a special courtship dance to attract the female. If the female appreciates the dancing she may join him. Then they join their bodies together end to end at their abdomens. Here, the male passes the sperm to the female's egg-laying tube, which will soon be fertilised by the sperm. [154]

Many animals make plugs of mucus to seal the female's orifice after mating. Normally such plugs are secreted by the male, to block subsequent partners. In spiders the female can assist the process. [155] Spider sex is unusual in that males transfer their sperm to the female on small limbs called pedipalps. They use these to pick their sperm up from their genitals and insert it into the female's sexual orifice, rather than copulating directly. [155] On the 14 occasions a sexual plug was made, the female produced it without assistance from the male. On ten of these occasions the male's pedipalps then seemed to get stuck while he was transferring the sperm (which is rarely the case in other species of spider), and he had great difficulty freeing himself. In two of those ten instances, he was eaten as a result. [155]

In the orb-weaving spider species Zygiella x-notata, individuals engage in a variety of sexual behaviors including male choosiness, mate guarding, and vibrational signaling in courtship. [156] [157]

Research into human evolution confirms that, in some cases, interspecies sexual activity may have been responsible for the evolution of new species (speciation). Analysis of animal genes found evidence that, after humans had diverged from other apes, interspecies mating nonetheless occurred regularly enough to change certain genes in the new gene pool. [158] Researchers found that the X chromosomes of humans and chimps may have diverged around 1.2 million years after the other chromosomes. One possible explanation is that modern humans emerged from a hybrid of human and chimp populations. [159] A 2012 study questioned this explanation, concluding that "there is no strong reason to involve complicated factors in explaining the autosomal data". [160] [ dubious – discuss ]

When close relatives mate, progeny may exhibit the detrimental effects of inbreeding depression. Inbreeding depression is predominantly caused by the homozygous expression of recessive deleterious alleles. [161] Over time, inbreeding depression may lead to the evolution of inbreeding avoidance behaviour. Several examples of animal behaviour that reduce mating of close relatives and inbreeding depression are described next.

Reproductively active female naked mole-rats tend to associate with unfamiliar males (usually non-kin), whereas reproductively inactive females do not discriminate. [162] The preference of reproductively active females for unfamiliar males is interpreted as an adaptation for avoiding inbreeding.

When mice inbreed with close relatives in their natural habitat, there is a significant detrimental effect on progeny survival. [163] In the house mouse, the major urinary protein (MUP) gene cluster provides a highly polymorphic scent signal of genetic identity that appears to underlie kin recognition and inbreeding avoidance. Thus there are fewer matings between mice sharing MUP haplotypes than would be expected if there were random mating. [164]

Meerkat females appear to be able to discriminate the odour of their kin from the odour of their non-kin. [165] Kin recognition is a useful ability that facilitates both cooperation among relatives and the avoidance of inbreeding. When mating does occur between meerkat relatives, it often results in inbreeding depression. Inbreeding depression was evident for a variety of traits: pup mass at emergence from the natal burrow, hind-foot length, growth until independence and juvenile survival. [166]

The grey-sided vole (Myodes rufocanus) exhibits male-biased dispersal as a means of avoiding incestuous matings. [167] Among those matings that do involve inbreeding the number of weaned juveniles in litters is significantly smaller than that from non-inbred litters indicating inbreeding depression.

In natural populations of the bird Parus major (great tit), inbreeding is likely avoided by dispersal of individuals from their birthplace, which reduces the chance of mating with a close relative. [168]

Toads display breeding site fidelity, as do many amphibians. Individuals that return to natal ponds to breed will likely encounter siblings as potential mates. Although incest is possible, Bufo americanus siblings rarely mate. These toads likely recognise and actively avoid close kins as mates. Advertisement vocalisations by males appear to serve as cues by which females recognise their kin. [169]


EVOLUTIONARY SCENARIOS

In speculating on the evolutionary origins of human sexual behavior, Charles Darwin noted, in Sexual Selection, and the Descent of Man, “Humans would probably have lived, as already stated, as polygamists or temporarily as monogamists. Their intercourse, judging from analogy, would not then have been promiscuous. They would, no doubt, have defended their females to the best of their power from enemies of all kinds, and would probably have hunted for their subsistence, as well as for that of their offspring. The most powerful and able males would have succeeded best in the struggle for life and in obtaining attractive females.” Darwin's observations are consistent with many aspects of contemporary theorizing concerning the evolution of male mating strategies they leave out female strategies, which can be better elaborated, as we shall see below.

In this section, I discuss evolutionary scenarios concerning hominin sexual behavior. Phylogenetic insights are drawn from great ape comparisons, specifics of the hominin fossil and archaeological record, and insights into recently studied human hunter-gatherer societies, with overarching theoretical guidance provided by sexual selection theory and socioecological principles. These scenarios will also later be connected with genetic and physiological data, contemporary international studies of human sexual behavior, and insights drawn from a life course perspective on human sexuality. While there is ongoing debate about specific evolutionary models of hominin sexuality, not surprisingly in light of the limitations of available data, it is also worth underscoring that the models are consistent with these latter bodies of evidence, an indication that there is a coherent and synthetic science here.

Early hominin and australopithecine sexuality

Current genetic and fossil evidence suggests that the closest living relatives of humans are chimpanzees and bonobos (Goodman et al., 1998 ). Genetic data suggest that chimpanzees and bonobos themselves had a last common ancestor in Africa about 1 million years ago (Prufer et al., 2012 ). Humans had a last common ancestor with chimpanzees and bonobos in Africa around 6 million years ago. What was that ancestor like, and what can we infer about its sexual behavior? As we shall see, there are clues to help answer these questions, but there are also uncertainties.

The earliest putative hominin fossils indicate body sizes comparable to today's chimpanzees and bonobos (Senut et al. 2001 Brunet et al., 2005 Lovejoy, 2009 ). The finds are all in Africa. The locomotor anatomy suggests the earliest hominins, as well as later gracile and robust australopithecines, were semiterrestrial bipeds. They retained both adaptations for spending time moving in trees (e.g., long finger bones, relatively long arms, and mobile shoulder joint) and for moving bipedally. Most models suggest they moved bipedally on the ground (Lieberman, 2011 ), although it has also been suggested that bipedalism emerged on tree branches during foraging (Crompton et al., 2008). The environmental reconstructions of early and later pre-Homo hominins suggest they inhabited wooded environments. A few early hominins, such as a find at Chad dated to approximately 7 million years ago, appeared to have slightly larger canine teeth (compared with modern humans, but less than great apes), though generally among hominins canine teeth are reduced in size compared with extant and presumably ancestral great apes. The shift toward greater bipedalism may have relaxed selection on retention of larger canine teeth, particularly among males, for use in male–male contest competition fighting may have relied, instead, on punching, grappling, or use of weapons.

If early hominins were similar to extant great apes, these early hominins likely mated primarily diurnally (see Mitani et al., 2012 ). Among contemporary chimpanzees, most matings in the wild occur early morning or late afternoon when chimpanzee groups are more fused compared with other times across the day when they may be more fissioned (Martin Muller, personal communication). Most sexual behavior was likely in a type of ventral-dorsal position (e.g., males from behind), although bonobos and orangutans are recognized to use a wider array of sexual positions, especially compared with other primates and mammals (Dixson, 2012 ). Based on great ape comparisons, most matings likely took place on the ground. If early hominin sexuality resembled that of chimpanzees and bonobos, then it would have entailed mating in multimale, multifemale groups. Further, early hominin females might have mated with many males, while also showing preferential mating access to a dominant male around the time she was most fertile. Females might have mated during parts of their pregnancy, but exhibited profound reductions in sexual behavior when in a state of postpartum lactational amenorrhea (i.e., not cycling, but heavily lactating and caring for an infant). Males may have competed heavily through alliance formation and contest competition with other males for social rank, in turn translating higher rank into greater mating success. At this time, it is difficult to discern whether chimpanzees, some other ape such as gorilla, or no extant ape can serve as a strong referential model for early hominin sexuality. Reasons for the lack of clarity include questions whether the multimale, multifemale mating system of chimpanzees and bonobos (and related traits such as exaggerated sexual swellings and heightened evidence of sperm competition) is derived or shared with a common ancestor over reconstructions of the degree of body size sexual dimorphism among early hominins and australopithecines and a dearth of relevant genetic analyses that might be able to address the evolutionary polarity of potential shifts in hominin sexuality.

Most researchers suggest that australopithecines were more polygynous than members of the genus Homo (McHenry, 1994 ). Debate continues on the number of gracile australopithecines and their phylogenetic relationship to earlier hominins and later members of Homo (Wood and Lonergan, 2008 ). However, most reconstructions of the postcranial remains of gracile australopithecines suggest they exhibited greater degrees of body size sexual dimorphism compared with modern humans and most other members of Homo, and possibly even more dimorphism compared with chimpanzees and bonobos (see Plavcan, 2012 ). The available postcranial remains are scanty, are scattered across time and locations, and entail inferences regarding sex in the first place. Such considerations have led other researchers to question whether australopithecine body size dimorphism estimates were exaggerated. It has been suggested the Aust. africanus might have been less dimorphic than Aust. afarensis (Harmon, 2009 ). It has also been suggested by Reno et al. ( 2003 ) that gracile forms were only mildly dimorphic—comparable with modern humans. If gracile australopithecines were highly dimorphic, the theoretical inference would suggest they mated in one-male polygynous groups, perhaps somewhat similarly to gorillas (Geary and Flinn, 2001 ). If they were only mildly dimorphic, that suggests, instead, they were mildly polygynous, and perhaps mating in somewhat human-like ways from this earlier time. The robust australopithecines, which most scholars suggest became evolutionary side branches rather than serving as human ancestors, appeared to be highly sexually dimorphic in body size. Aust. robustus, from southern Africa, may have had pronounced sex differences in reproductive maturation, consistent with one-male polygyny (Lockwood et al., 2007 ), and appeared to exhibit sexually dimorphic craniofacial anatomy, also consistent with some degree of polygyny (Lockwood, 1999 ). Attempts to draw additional inferences concerning hominin sexuality have used the study of digit ratios (Nelson et al., 2011 ) and other aspects of craniofacial dimorphism (Schaefer et al., 2004 ), but without clear inferences. It can also be noted that the penis bone (baculum) and homologous clitoral bone were lost during hominin evolution, a difference consistent with evolutionary changes in our ancestors' reproductive anatomy (Dixson, 2009 ).

Sexuality in the genus Homo

Most evolutionary models of sexuality in the genus Homo suggest that grade shifts took place during early or middle Homo evolution. The transition from a presumed gracile australopithecine form to early Homo remains murky in phylogenetic and archaeological detail, in part because of a paucity of fossil material during this time frame. Scenarios regarding body size estimates and indices of sexual dimorphism are highly contingent upon availability of new and still-rare fossil specimens. For example, 1990s models suggested that Homo erectus/ergaster exhibited increases in body size, had lower (human-like) body size sexual dimorphism, and human-like limb proportions, with much of that inspiration drawn from the Nariokotome boy (KNM-WT-15000) (Walker and Leakey, 1993 ). More recently, a 1.5-Ma pelvis from Gona has been used to suggest that some females at that time were still small, and thus that body size dimorphism could have remained high, and similar to previous scenarios of highly dimorphic gracile australopithecines (Simpson et al., 2008 ). The shift toward human-like body proportions (e.g., relatively shorter arms), along with environmental reconstructions, suggests that Homo inhabited a wider array of environments than its woodlands-bound predecessors, and had also become a committed biped (giving up perhaps sleeping in trees at night). Beginning around 1.5 Ma, members of Homo began using new stone tool traditions, marked by the Acheulian (Foley and Gamble, 2009 ). Estimated brain sizes increased however, the limited availability of postcranial remains makes adjustment for body size difficult, and probably thus leaves early and mid Homo as less encephalized as later forms. Additionally, dental microstructure studies suggest that the pace of development was more apelike than human-like (Dean et al., 2001 ), providing further impetus for seeing grade shifts in Homo as still showing considerable change over time rather than being established quickly with the earliest forms.

Estimates of both Neandertal and modern human body size sexual dimorphism suggest about 15% differences in height and weight (see Plavcan, 2012 ). This would suggest modest degrees of male–male contest competition, consistent with slight polygyny/mostly monogamy. If this pattern held among the common ancestor of Neandertals and modern humans, then presumably similar aspects of sexual behavior held among archaic Homo/Homo heidelbergensis in Africa by about 600,000 years ago. Whether similar patterns can be pushed back to earlier Homo around 1.5 Ma then depends on the issues noted above regarding early Homo/Homo erectus skeletal material.

A socioecological approach to hominin sexuality

To orient potential evolutionary models of sexuality in the genus Homo, we can draw upon socioecological principles. See Figure 1 for graphical illustration of a basic socioecological model. Such principles in turn begin with Bateman's observations and additional layers concerning sex differences in reproductive constraint and reproductive strategy. As Wrangham ( 1979 ) noted, if females are ultimately constrained by access to resources such as food, then it makes sense in developing socioecological models of primate social behavior to ask about how females will distribute themselves in an environment with respect to available food resources. Van Schaik ( 1983 ) suggests that predation pressures may also serve as major selective forces operating on female distributions. Applied to the transition from a gracile australopithecine to early Homo, the shift toward committed, terrestrial bipedal lifeways might have exposed females to greater predation pressures (in terrestrial compared with arboreal environments). That could favor enhanced female group sizes. The formation of larger female group sizes could amplify female foraging competition. That could fuel intensified female extractive and processing foraging strategies, perhaps including tools used for digging roots (and tools that, incidentally, would not be regularly found in the fossil record, although some microwear studies of stone tools are also consistent with plant processing). If females are in larger groups, then they become more difficult for a single or several males to monopolize. From socioecological first principles, males are expected to map on to the availability of fertile females. With a larger number of males within groups, consequences could be diminished male reproductive skew, and perhaps male–male egalitarian relationships. The presence of multiple males in groups could foster lower-ranking males to attempt to mate guard fertile females, as is sometimes observed in chimpanzees, in which males attempt to coerce females into short-term liaisons removed from other group members. This kind of male mate guarding in Homo could give rise to long-term sociosexual relationships, but within multimale, multifemale groups.

One aspect of such modeling is that evolutionary shifts in hominin sexuality are theorized from principles applied to other primates. This is different from emphasizing human-specific arguments. Another aspect of this approach is that it sees social behavioral changes rooted in female foraging and male mate-seeking as the foundation, with subsequent layers of hominin economic and social behavior building on these. For example, a pronounced hunter-gatherer sexual division of labor is viewed as a more recent derivative of the preceding shifts in sexuality. Table 1 illustrates some leading models concerning the evolutionary foundations of Homo sexuality, featuring female perspectives, male perspectives, and commentary concerning the possible timing and relevance of each (see also Quinlan, 2008 ).

Model Female perspective Male perspective Timing and relevance
Mate guarding (Hawkes, 2004 ) No benefit constrained choice Aids paternity certainty Some relevance across Homo may have been the original basis of long-term Homo sociosexual partnerships, since in a wider phylogenetic scope male mate guarding is one of the best predictors of social monogamy (Lukas and Clutton-Brock, 2013 ) female hunter-gatherers favor specific mates and often seek to maintain a bond
Hired Gun (Mesnick, 1997 ) Reduced predation and/or coercion by others of self and offspring Benefit from sexual access in exchange for offering protection Some relevance across Homo while male partners tend to be the most coercive of female partners, those same male partners may also deter additional coercion by other males and have helped reduce predation upon females and their offspring
Infanticide avoidance (van Schaik and Dunbar, 1990 ) Reduced risk of infanticide if bonded to a protective male May benefit from sexual access and higher offspring survival Some relevance if early hominins or Australopithecus lived in one-male groups, in which infanticide risk tends to be higher little evidence of infanticide risk by unrelated males among hunter-gatherers
Food-for-sex (Fisher, 1982 ) Benefit from food Benefit from sexual access May be part of the sex-specific resource exchange within long-term unions and within a sexual division of labor
Male provisioning (Kaplan et al., 2000 ) Gain from food resources in a sexual division of labor Gain from mating access with a long-term partner within a sexual division of labor Relevance to recently studied hunter-gatherers, but unlikely to be the starting point of Homo shifts to long-term sociosexual bonds
Cooking hypothesis (Wrangham et al., 1999 ) Benefit from reduced theft of cooked foods Gain mating access in exchange for protection Evidence of regular use of fire/cooking aligns best with archaic Homo/Homo heidelbergensis evidence for hunter-gatherer concern over food theft is lacking could be consistent with other protective services
Exchange of mates under parental control (Apostolou, 2007 Chapais, 2008 ) Expands social ties and provides a mate, but with potential parent-offspring conflict Gains expanded social ties and a mate, but with some potential for parent-offspring conflict Relevant to recently studied hunter-gatherers unlikely to project beyond modern humans given cognitive and demographic constraints underlying mate exchange

Hunter-gatherer sexuality

As another source of insight into the evolution of human sexuality, we can draw upon patterns observed among recently studied hunter-gatherers (Berndt and Berndt, 1951 Shoskak, 1981 Hewlett and Hewlett, 2010 Marlowe 2010 Walker et al., 2011 ). Because the socioecology of hunter-gatherers is thought to resemble in some respects (e.g., small group sizes, family relationships) that in which earlier forms of Homo sexuality evolved, hunter-gatherers can serve as analogies for more distant patterns. Of course, recently studied hunter-gatherers are not living fossils they have different foraging tools than more distant ancestors (e.g., Marlowe, 2005 ), among other differences. Yet observations and patterns among foragers offer insights that otherwise are not accessible.

From recently studied hunter-gatherers, the most common marital system is slight polygyny (Marlowe, 2005 Walker et al., 2011 ). That is, among foragers, most societies allow polygyny, but typically only a few men are married polygynously, with the vast majority of men monogamously partnered. The regional exception is among Australian aborigines, where higher rates of polygynous marriage were observed, but that may be in part due to cultural transmission from New Guinea (see O'Connell and James 2007). Across hunter-gatherers, the men most likely to have two wives tend to have higher status, achieved through hunting success or from shamanic activities (Smith, 2004 ). Divorce is variably common, especially among younger couples (Blurton Jones et al., 2000 Winking et al., 2007 ). Marriages, especially first marriages, are often arranged by older family members, although the married partners may have influence on whether those arrangements proceed (Apostolou, 2007 ). While polyandrous mating systems tend to be rare in mammals generally, including humans, it is occasionally observed among hunter-gatherers, and typically when there is a shortage of men (Starkweather and Hames, 2012 ). Affairs also occur, with love triangles (e.g., men competing over a woman) a regular context of competition among foraging societies such as the !Kung and Hadza (Gat, 2006 ).

What other aspects of hunter-gatherer sexuality stand out? A sexual division of labor is observed, whereby females tend to undertake subsistence activities yielding reliable food availability and in ways compatible with having young children (Bliege Bird, 1999 Marlowe, 2007 ). Males tend to undertake riskier subsistence activities, including foraging for more difficult-to-acquire but highly relished foods such as larger game animals and honey. Foods may be shared between partners, with a female's provision of reliable resources helping make possible a male's riskier undertakings. Resources males acquire appear designed to serve multiple ends: partly as provisioning family members, but with the acquisition and sharing of large game also enhancing male status in ways that may yield political benefits or mating opportunities (Marlowe, 2010 ). It has also been suggested that male resources are most useful during a “critical period” of provisioning a partner who has a young nursling (Marlowe, 2003 ).

Also among hunter-gatherers, females spend the bulk of their reproductive years pregnant or in a state of lactational amenorrhea, meaning that they are nursing but not cycling (Short, 1976 Ellison, 2001 ). This latter observation has dramatic impacts on the evolutionary foundations of human sexuality: it is comparatively rare for a woman to be cycling, and the true female baseline is one of fluctuations in sexuality across reproductive states. Among foragers, there are also few unattached and fertile females. Individuals are familiar, and frequently off-limits as potential mates because they are close family members or circumscribed for other reasons that may be designed to extend coalitions (e.g., wife exchange). One of the distinguishing features of hunter-gatherer sexuality (and among humans more generally) compared with other primates is that sex is typically covert. While in some other primates surreptitious matings may take place to reduce same-sex conflict or coercion (e.g., baboons: Smuts 1985 ), this is a much greater human concern. Ethnographic descriptions include cases of couples having sex at night near a fire, within short distance of children and other campmates (but the poor light providing some cover) in other cases, a couple may seek to have sex during the day away from camp. One interpretation of the pattern of seeking to shield sexual behavior from the eyes of others is that it may reduce sexual jealousy and mating competition. The unusual human mating pattern of forming long-term sociosexual bonds within multimale, multifemale groups is vulnerable to such competition. This privacy-seeking also contrasts with the sexual behavior of other apes, in which group members often have abilities to witness the sexual behavior of group-mates. Additionally, same-sex sexual behavior has been observed among some, but not all, hunter-gatherer societies (Hewlett and Hewlett, 2010 ). Few details of forager sexuality across the life course are available: sex play has been reported in several foraging societies, including the !Kung, Hadza, and Aka, while among the Aka older couples have sex less frequently (Hewlett and Hewlett, 2010 ).

Summary

Evidence from other primates, the hominin fossil and archaeological record, and studies of human hunter-gatherers can be combined with socioecological principles to depict the evolution of hominin sexuality. There are a range of theoretical models to draw upon in this effort, such as models emphasizing the benefits of male protection or care to long-term bond formation. Some reconstructions of early hominin sexuality draw upon comparisons with chimpanzees because they and bonobos are our closest living relatives and the body sizes of early hominins are chimpanzee-sized. However, debate continues whether features of the multimale, multifemale mating system of chimpanzees are derived or shared with an early hominin. Many reconstructions of gracile australopithecine sexuality feature pronounced body size sexual dimorphism, which could be consistent with gorilla-like one-male polygyny other reconstructions emphasize more modest dimorphism. Most scenarios suggest that body size dimorphism decreased in early or mid Homo evolution, with the inference that these hominins experienced lower male–male contest competition and more socially monogamous long-term bonds. The transition toward slightly polygynous/more monogamous Homo may have originated with changes in female foraging and possibly increased group sizes, attended by male mate guarding. During later Homo, male care, in particularly provisioning, may have arisen, reinforcing benefits such as higher female lifetime reproductive success and male sexual access to forming long-term bonds. Among modern humans, older adults may have taken on greater and evolutionarily novel roles in mate exchange. Across the existence of long-term hominin sociosexual bonds, male protection against harassment by other males may have been relevant, although aspects of the infanticide and cooking models are less supported. Key features of human sexuality thus arose in a mosaic fashion during hominin evolution, with different selective scenarios having relevance at different times.


Discussion

The results presented here (a) provide the first empirical demonstration of women systematically producing higher-variance economic returns than men from the same society and (b) show that the assumptions of the economy of scale model of the sexual division of labour can explain the circumstances associated with Shodagor women's trading, which produces high-variance returns and is not compatible with childcare, as well as those associated with women's occupations (fishing, housewife) that follow cross-cultural trends more closely. Results support predictions that women who trade will be unconstrained by intensive demands of childcare through weaning and alloparental care, that complementary childcare provided by fathers is critical in addition to care from alloparents and that Shodagor women's trading is associated with comparative advantages. While it is not always the case that a particular occupation or subsistence strategy is incompatible with childcare and associated with high levels of economic risk, both characterize Shodagor women's trading. We discuss which of our results may be more directly related to each aspect of trading and how a more general model of the sexual division of labour may predict these aspects of women's work across societies.

Removal of childcare constraints predicts trading

Any adult who does not need to care for small children for the majority of the day is free to pursue economic or subsistence strategies that are incompatible with childcare. Weaning is a process whereby women can free themselves from the demands of suckling, and cross-cultural research shows that women often do so in order to return to work (Schwartz et al., Reference Schwartz, d'Arcy, Gillespie, Bobo, Longeway and Foxman 2002 Motee et al., Reference Motee, Ramasawmy, Pugo-Gunsam and Jeewon 2013 Sellen, Reference Sellen 2001 Levine, Reference Levine 1988). As predicted, our results show that, in most cases, Shodagor women whose children were fully weaned in 2014 were more likely to work as traders than to fish or be housewives. However, there is some uncertainty around the magnitude of this effect. The most likely explanation for this is that the variable used here reflects whether or not each woman was breastfeeding at all at the time of the interview, but not the frequency of suckling, which should have differential impacts on a woman's ability to trade. For example, a woman who is exclusively breastfeeding and is her child's only source of nutrition is likely to be far more constrained than one whose child only breastfeeds a few times per day and gets most of his or her nutrition from solid foods. We expect that a more detailed examination of the relationship between breastfeeding frequency and work would reveal more nuanced decision-making among women with young children. Regardless, these results indicate that the temporary constraints of intensive breastfeeding are not sufficient to keep women from ever participating in economic tasks that are incompatible with childcare.

In addition to weaning, a mother must also have alternative caregivers available to watch her children while she works. Alternative caregivers are also a necessity for fathers to engage in childcare-incompatible economic tasks, but the economy of scale model assumes that maternal care fills this need. Thus, we predicted, and the data show, that complementary care from a spouse is an important predictor of Shodagor women's trading. Instead of fishing or earning money as day labourers, some fathers stay at home during the dry season to be primary caregiver for young children while their wives are working. Although the amount of paternal care among Shodagor households has not yet been formally quantified, women who trade often work 5–7 days per week for 8–10 hours per day and fathers who care for children during this time report engaging in childcare the majority of the day. Compared with cross-cultural reports of paternal care, these Shodagor men appear to be at the very high end of time spent with children (Marlowe, Reference Marlowe 2000).

While there may be more cases of systematically high levels of paternal care than are quantified or represented in the behavioural ecology literature (e.g. Livingston, Reference Livingston 2014 Milgram, Reference Milgram and Seligmann 2001 OECD, 2017), the overwhelming cross-cultural norm for paternal care appears to be one of low direct investment relative to mothers. For Shodagor families, high rates of paternal care probably represent a behavioural adaptation to a unique ecology, which includes a high risk of drowning for young children. Among the majority population in Matlab, 40% of deaths of children between the ages of 1 and 4 years were due to drowning in 2016 (ICDDRB, 2016). A nationwide study from 2003 shows an even higher rate of death for that age group (Rahman et al., Reference Rahman, Mashreky, Chowdhury, Giashuddin, Uhaa, Shafinaz and Rahman 2009). Over 35% of children who drowned did not have a specified caregiver, and of those who did, 52% had caregivers who were under the age of 15. In contrast, in qualitative interviews, Shodagor adults report that child drowning is not a major cause of child death in their communities, which suggests that their caregiving strategies are effective. Under different socioecological circumstances, we might see that women do childcare-incompatible work when they have older children who are able to be left at home with minimal supervision (e.g. Starkweather, Reference Starkweather 2017) or when alloparents can substitute the majority of daily care for younger children (e.g. Ivey, Reference Ivey 1993 Reference Ivey 2000 Meehan, Reference Meehan 2008 Quinlan, Reference Quinlan 2003). In both cases, we would still expect time spent in childcare by mothers and fathers to be somewhat complementary in that fathers should increase the amount of direct care to make up for lost care by mothers, as has been shown among Aka fathers (Hewlett, Reference Hewlett 1991).

While complementary care from a spouse is important in this case study, we also expect alloparents to play a role in allowing women to do work that is not compatible with childcare. The reality for most families in most societies – even when the mother is the primary caregiver of children – is that children are cared for by a constellation of different people, including mothers, fathers and alloparents (Meehan et al., Reference Meehan, Helfrecht, Malcom, Meehan and Crittenden 2016). Indeed, our results show that having more alloparents available increased the likelihood that a woman would trade. The independent importance of fathers and alloparents suggests that both are key in allowing women to trade and indicates three possible caretaking scenarios: (a) either one type of caregiver or the other (fathers or alloparents) is doing the vast majority of care (b) fathers and alloparents work together to create a patchwork of daily caregivers for children or (c) one type of caregiver provides daily care for younger children and another for older children. Shodagor families probably represent a combination of these scenarios. Among Agta families, when mothers are engaged in other activities, alloparents appear to do the majority of intensive childcare (e.g. holding) and fathers do less-intensive types of care (e.g. watching, proximity Page et al., Reference Page, Viguier, Emmott, Dyble, Smith and Migliano 2019). Some Shodagor trading families display a similar pattern but with fathers doing the bulk of daily care and alloparents providing supplementary care. The choice of caregiver(s) and the amount of time dedicated to caretaking by fathers and alloparents probably varies over time and between families depending on multiple factors that include a household's economic need, alloparents’ alternative commitments (e.g. work, caring for other children) and child age.

Ecological and cultural comparative advantages in trading

While weaning and allomaternal care providers allow women to engage in economic tasks that are not compatible with childcare, they may not be sufficient to explain women's engagement in a high-risk economic activity. The economy of scale model, as originally written (Becker, Reference Becker 1985), suggests that men's pursuit of risky economic tasks is a byproduct of the complementary nature of their work, which is a response to women's comparative advantages in childcare. Gurven and colleagues (2009) later suggested that opportunity costs associated with particular activities should also play a role in risk pursuit. We suggest that, rather than risk being a byproduct of work that is incompatible with childcare, comparative advantages in a high-risk task, which take opportunity cost into account, and the complementary pursuit of low-risk resources by a spouse, should allow individuals of one gender to systematically engage in the high-risk task.

The economy of scale model focuses on the comparative advantage that women are afforded by their biological ability to gestate and lactate, but we should expect comparative advantages to stem from other sources, too, including the local socioecology. Ecological settings influence selective pressures on sex differences among various species in provisioning and direct parental investment (Scharer et al., Reference Scharer, Rowe and Arnqvist 2012). The local ecology also influences the resources that are available for human use, as well as seasonal availability of and opportunity costs associated with different resources. Seasonality (Marlowe, Reference Marlowe 2007) and energy/risk tradeoff (Codding, et al., Reference Codding, Bliege Bird and Bird 2011a) associated with resources that are available in certain ecologies may also affect how labour is divided by gender. Our data show that important aspects of the Shodagor ecology – distance to a major market and distance to the Meghna River – distinguish among the primary occupations women choose to pursue. Women are more likely to trade if they live closer to a major market and farther from the Meghna River. Each of these ecological features represents different opportunity costs for women. Living near a market reduces the amount of travel time between home and the middleman's shop, which traders visit in the morning to pick up their basket and in the evening to drop it off. Living farther from the Meghna River increases costs to fishing – especially during the dry season when fish are less abundant farther from the Meghna. Earlier analyses also showed that women who fish were more likely to live near the Meghna, where fishing is profitable year-round (Islam & Chuenpagdee, Reference Islam, Chuenpagdee, Johnson, Acott, Stacey and Urquhart 2018 Figure S1). These results indicate that women are sensitive to opportunity costs associated with local ecological features when choosing an occupation. They also suggest that comparative advantage in a risky activity may be born from opportunity costs, as predicted by Gurven and colleagues (2009), but that factors beyond biological sex differences should be considered in order to understand gender differences in pursuit of economic risk.

Of course, Shodagor men – in fact, everyone living in Matlab – should be sensitive to the same costs and benefits. However, comparative advantage in an activity associated with high economic risk may also be associated with aspects of culture. Zapotec women traders primarily sell products to other women in marketplaces, operating within an economic sphere open exclusively to women by custom (Chinas, Reference Chinas 2002). Similarly, haenyeo women divers in South Korea reportedly took over diving tasks from men in the seventeenth century because women's wages were not subject to taxation (Hilty, Reference Hilty 2015). Likewise, Shodagor women traders report a comparative advantage over men and over non-Shodagor women related to cultural rules and expectations of the majority Muslim population in Bangladesh. The majority of rural Bangladeshi women who are not Shodagor follow rules of seclusion, or purdah (Amin, Reference Amin 1997), which limits the contact of women with men outside of their families, while most Shodagor women do not follow these rules. It is thus culturally acceptable for non-Shodagor women to interact with other women, even without a male relative present, but it is not acceptable for them to interact in the same way with an unknown or unrelated man. Shodagor women report that this allows them to fill a niche as traders, trading door-to-door to women in remote villages who rarely have the opportunity to visit the market, whereas men (whether Shodagor or not) would be unable to fill this role.

In short, ecological and cultural comparative advantages in Bangladesh converge to create a niche only available for a subset of Shodagor women to fill. The occupation associated with the niche produces high levels of economic risk. Although we expect comparative advantages to be context-dependent, our results show that they need not be based exclusively on biological sex differences in order to explain a wide range of divisions of labour by gender.

Complementary risk strategies

High levels of variance in nutrient and caloric intake can be detrimental for children's health and well-being (e.g. Cook et al., Reference Cook, Frank, Berkowitz, Black, Casey, Cutts and Nord 2004 Gundersen & Kreider, Reference Gundersen and Kreider 2009 Gundersen & Ziliak, Reference Gundersen and Ziliak 2015), therefore, we expect parents to provide children with reliable calories as often as possible. The economy of scale model suggests that when resources are pooled at the household level, higher-variance returns – usually pursued by fathers, which may also provide complimentary nutrients – are offset by mothers’ provisioning of reliable resources, and work together to support child health and well-being (Gurven et al., Reference Gurven, Winking, Kaplan, von Rueden and McAllister 2009). Therefore, we expected that Shodagor women's higher-variance returns from trading would be offset by husbands’ reliable fishing returns. Our model results do not formally support this prediction: men's economic risk (CV) does not differ based on wife's occupation (Figure 2). However, our results also do not necessarily contradict our prediction. In fact, we show that the fishing methods used by all Shodagor people produce relatively reliable, low-variance returns (Figure 1), so there may be little difference between husbands based on wife's occupation simply because there is little variation in returns to this occupation in general.

When considering the potential for complementarity in risk strategies between spouses, it is also necessary to take into account tradeoffs associated with market integration. While over 80% of Shodagor households engage in subsistence fishing occasionally, a large majority of fish are sold in markets in exchange for the local currency, BDT. Traders also exchange goods for cash. Unlike the resources acquired in ‘immediate-return’ systems experienced in some foraging societies (e.g. Woodburn, Reference Woodburn 1982), money is ‘both storable and fungible’ (Gurven et al., Reference Gurven, Jaeggi, von Rueden, Hooper and Kaplan 2015), meaning it can be saved and used at a later date to buffer against future resource shortfalls. It is likely that excess income earned by traders (i.e. income not used the same day it was earned) is saved and later spent on days when not enough is earned to cover the household's expenditures. Indeed, high-mean returns on trading would also alter tradeoffs associated with higher variance (Jones et al., Reference Jones, Bliege Bird and Bird 2013). However, our model shows that trading is associated with a lower average daily income than fishing (Figure S2), and raw data indicate that traders earned an average of 262 BDT per day in 2014 (the equivalent of around 3.00 USD), while fishers earned an average of 652 BDT per day (approximately 7.70 USD). This suggests that traders are much less likely than fishers to have excess income at the end of the day and therefore less likely to use their own income to buffer against later shortfalls. Instead, multiple Shodagor families report saving fishing income from the rainy season to use during the dry season, indicating that modelling a husband's economic risk-taking may not be sufficient to understand complementarity in spousal risk strategies, nor economic motivations underlying Shodagor women traders’ pursuit of a high-risk occupation. Future research will examine the cross-seasonal nature of risk buffering in Shodagor households, including the impact of a husband's (or husband and wivfe's joint) rainy season earnings on a wife's dry season economic risk-taking.

In Shodagor trading households, the possible excess of a storable resource (i.e. money) produced by men's fishing should be critical in shaping women's risk sensitivity primarily because fishing and trading are done during opposite seasons. We expect the low-variance nature of fishing to be important during the rainy season when the majority of household resources are a product of fishing, but the ability to save money to buffer against women's risk-taking may be critical during the dry season. In other cultural contexts, when occupations switch seasonally and in a manner similar to what Shodagor families experience, we expect women's sensitivity to variance to be structured according to access storable resources saved from previous seasons. However, for contexts in which men and women engage in occupations with different risk profiles at the same time, women's pursuit of variance should be related to men producing lower-variance resources and not to men producing an excess of resources, or the storability of those resources. Overall, these results suggest that, in contexts where men's primary occupation is associated with low-variance returns, and possibly also when it produces an excess of storable resources (e.g. money), women could be in a strong position to pursue higher-risk tasks when ecological and cultural circumstances allow.

Limitations

This study has a few limitations. First, while we show support for predictions based on the economy of scale model, we do not have the data necessary to adequately test the ability of other models of sex- or gender-role specialization to explain the variety of gendered labour patterns among Shodagor families (e.g. Bliege Bird & Bird, Reference Bliege Bird and Bird 2008 Fromhage & Jennions, Reference Fromhage and Jennions 2016 Henshaw et al., Reference Henshaw, Fromhage and Jones 2019 Lehtonen et al., Reference Lehtonen, Parker and Scharer 2016 McNamara et al., Reference McNamara, Szekely, Webb and Houston 2000). Future work will explore possible alternative explanations for Shodagor gendered division of labour, including effect of sex ratio or mating competition, and evidence of social benefits from trading.

Second, the cross-sectional nature of this dataset makes it difficult to determine the direction of causality between a woman's occupation and her socioecological circumstances. While we would expect most of the variables we measure to adjust in real time to a woman's occupation (e.g. a man could adjust his economic risk-seeking to meet his wife's), ecological variables are more difficult to interpret in this respect. We do not know if a family chose their location based on a woman's occupation, or if she chose her occupation in response to the location of her family's residence. The mobility of boat-dwelling families further complicates interpretation, as mobility should allow households to change locations in order for women to engage in a particular occupation. However, self-selection into ecological circumstances associated with lower opportunity costs for an economic task does not negate the importance of the comparative advantage women experience. There is also little evidence from other data collected in 2014 to suggest that many families are moving in order for women to change occupations. So, despite potentially confounding factors of cross-sectional data and mobile households, we suggest that ecological comparative advantages provide a proximate explanation for Shodagor women's occupational decisions.


Hormones associated with various non-human primate reproductive behaviors: What they can teach us about ourselves

The endocrinology associated with reproduction is conserved among humans and non-human primate species because of our shared common evolutionary ancestry. Non-human primate species exhibit various reproductive behaviors that are mediated by different types of steroid hormones such as sexual swelling, social dominance by sex, promiscuous mating, and infanticide. Both the presence and the appropriate concentration of steroid hormones are vital to the effectiveness of each reproductive behavior. Some reproductive characteristics are sex specific while others are more complex and are affected by stress levels and social status. By researching the reproductive endocrinology of non-human primates, we can better understand the reproductive capacity of captive populations, with broader implications concerning our own reproductive physiology. Here, I 1) review the relationship between various steroid hormones and associated reproductive characteristics of non-human primates, and 2) emphasize the vast amount of knowledge we can gain from them, which includes understanding how to circumvent issues concerning our own fertility.

Introduction

The survival of a species depends on their ability to transfer their genetic material successfully to many offspring. Species utilize different reproductive characteristics evolved from their ancestors and reflect their life history traits to facilitate this process. Some of these characteristics are sex-specific, permitting animals to increase their fitness and to reproduce successfully. Social status can also dictate successful reproduction for animals in hierarchical societies, with dominant individuals having more advantages than subordinates. Hormones can mediate the expression of these characteristics and associated behaviors. By revealing the function of these hormones in non-human primates, we can illuminate their role in reproductive processes of other organisms that reproduce sexually, as well as their potential usage in drugs for regulating breeding and fertility in both primates and humans. The aim of this review is divided into two segments: First, I review the hormones of reproduction and address the question: is it merely the presence of certain reproductive hormones or the interaction between them that determines reproductive success in non-human primates? Second, I review the costs and benefits of incorporating non-human primates in research studies of reproduction, as well as the limitations, to identify the reasons why studies of non-human primates are useful in assembling information and broadening our understanding about various aspects of human reproduction and physiology.

I. Reproductive Characteristics of Various Primates

To reproduce successfully, non-human primates have evolved various characteristics and behaviors. Males and females tend to differ in the mechanisms they use in order to communicate to the opposite sex to let them know their reproductive status. It appears as though some reproductive behaviors have been conserved between various primate species, as well as the hormones associated with them, but the way in which the hormones function may vary from species to species, or even between individuals within the same species. The reproductive behaviors that have been heavily observed in non-human primates include sexual swelling, social dominance, promiscuous mating, and infanticide. Most of these behaviors are driven by the functioning of certain reproductive hormones that can be studied and used for analytical research for advances in breeding and fertility of non-human primates, as well as establishing correlations of reproductive hormones in primates and humans. Although infanticide involves the killing of offspring, it has been observed in various non-human primate species, mainly amongst males, as a way to curtail the momentary sterile phase of females whose ovulation is hindered from nursing their young (Boer and Sommer, 1992). In other words, females who no longer have to nurse offspring have a tendency to begin their ovulation cycle so that they can conceive again.

Sexual skin

Physical display of one’s reproductive status is one reproductive characteristic that is observed, mostly in female non-human primates. These physical displays range from sexual swelling of the skin or female genitalia to coloration of their perineal region (Nunn et al., 2001). Females who use this characteristic display these sexual signals during their menstrual cycle at a time when they are most likely ovulating (Nunn et al., 2001). Sexual swelling appears to be most prevalent in species in which females tend to live in social groups and have multiple mates. This phenomenon of reddening and swelling is a sexually selected trait that increases female attractiveness to potential mates and heightens male sexual arousal (Deschner et al., 2004). Additionally, females must compete for access to mates just as much as males do (Nunn et al., 2001). This particular form of achieving reproduction has been conserved among certain species mostly because it is a physical feature openly displayed by females that inform males of their reproductive status. Thus, females showing sexual swelling are more likely to attract attention from males and ultimately be enticed into mating with them. Some species that utilize this reproductive characteristic include chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla beringei), and white-handed gibbons (Hylobates lar).

Sexual Swelling: Chimpanzees

Researchers wonder why female chimpanzees have developed a visual form of sexual communication. One hypothesis states that exaggerated swelling results in male-male competition, allowing females to identify and mate with the fittest males (Nunn et al., 2001). Another hypothesis states that the exaggerated swelling of females attracts multiple males as mating partners, which most likely leads to paternity confusion and reduces the risk of infanticide, to be discussed later on (Nunn et al., 2001). These hypotheses support the notion that female sexual swelling signals to males’ reproductive receptivity, which typically causes different forms of relationships to occur.

Field studies show that both possessiveness and consortship appear to be the optimal mating relationships for both males and females due to the fact that the former gives males the highest probability of reproductive success, and the latter gives females the opportunity to exercise choice (Tutin, 1979). The formation of relationships could also be due to the fact that for the duration of the short-term relationship, neither partner has to compete with their same-sex counterparts, which increases the male’s chance of successful conception. These relationships that include female choice highlight the importance of sexual selection, which is arguably driven by the physical display of sexual swelling in females. Sexual swelling in female non-human primates is thought to reflect changes in the levels of estrogen and progesterone release, specifically during the menstrual cycle (Deschner et al., 2004). Maximum sexual swelling occurs during ovulation, at which estrogen levels significantly increase while progesterone levels remain at baseline (Deschner et al., 2004). Recently, two hypotheses have been established and debated over the significance of sexual swelling: females compete with one another for access to mates in a multi-male group and so perhaps the size of her swelling is an indication of her fitness (Deschner et al., 2004). Also to consider, swelling size could cause variability in the chances of conception due to the eccentric patterns of ovarian hormones (Deschner et al., 2004).

A field study reported that the timing of swelling detumescence (reduction) is correlated with ovulation, which is the most opportune time for conception (Deschner et al., 2004). However, it is unknown whether ovulation occurs toward the beginning or end of sexual swelling. It can be deduced that the sexual swelling occurs in concert with ovulation, mediated by the reproductive hormones estrogen and progesterone (Deschner et al., 2004). This study analyzed the role of these hormones in sex and conception of wild female chimpanzees. Deschner et al.’s study included free-living, unprovisioned female chimpanzees in three study populations in East Africa. Endocrine sampling included both urine and fecal samples. Urine samples were analyzed for estrogen conjugates and pregnanediol-3-glucuronide, and fecal samples were analyzed for estradiol and progesterone (Deschner et al., 2004). Deschner et al.’s study revealed that although hormone levels can change, a relationship was present between steroid concentrations from same day extractions. Deschner et al.’s results show a variability in timing of steroid secretion and swelling within the female chimpanzees of these three populations. Plasma estrogen peaked at 7–8 days prior to reduced swelling, but remained elevated until drastically declining at detumescence this result was seen in both nulliparous and parous females as well as for conception and non-conception cycles (Deschner et al., 2004). Nulliparous females have never given birth while parous females have offspring-reared at least once. Variability in timing and magnitude of peak levels was also observed for progesterone. Female chimpanzees had low progesterone levels during estrogen peak of follicular phase, followed by elevation in progesterone within the first 9 days of detumescence (Deschner et al., 2004). Deschner et al’s results supported one of the hypotheses, specifically that the period of maximal swelling should occur mid to late follicular activity since swelling of sexual skin is induced by estrogen, and that most luteal activity should occur after detumescence since progesterone activity reduces swelling in luteal phase (Deschner et al., 2004). These results suggest that the process of sexual swelling is driven by both the presence and the timing of peaks of these two hormones. Researchers also found significantly higher steroid conjugate levels in both the swelling and post-swelling phases of the conception cycles compared to the non-conception cycles (Deschner et al., 2004). Also, both the estrogen levels and the number of copulations with the alpha male significantly increased during the fertile period, throughout the duration of sexual swelling. Copulations peaked at

7 days before detumescence and remained elevated until the day of detumescence, which correlates to the time that estrogen peaks were elevated (Deschner et al., 2004). From this study, it can be concluded that both estrogen and progesterone are necessary to regulate the sexual swelling in female chimpanzees, but estrogen alone drives the sexual swelling (which attracts potential mates and leads to a higher chance of conception).

The fertility process in chimpanzees, one of our closest living relatives, can illuminate the notion that women evolved earlier fertility termination due to increased health risks in late births, according to Hawkes and Smith (2010). Thompson et al. (2007) contrasted age patterns of fertility in chimpanzees and humans, specifically two well-studied human foraging populations: the !Kung of Botswana and the Ache of Paraguay. They found that chimpanzees experience an earlier onset of fertility (10–14 years old), and reproduce more broadly across their life cycle compared to humans (Thompson et al., 2007). The !Kung population had peak fertility rates similar to chimpanzees, and there was no significant difference found between the age-dependent decline in chimpanzee fertility after age 25 from both human populations (Thompson et al., 2007). They also found that human reproduction ends when mortality is very low, while the fertility in chimpanzees declines at a similar pace to the decline in survival probability (Thompson et al., 2007). The similar patterns of declining birth rates observed between humans and chimpanzees suggest that the physiology of reproductive senescence was likely conserved in human evolution (Thompson et al., 2007).

Sexual Swelling: Gorillas

Another non-human primate species that utilizes sexual swelling of the skin as a reproductive characteristic are gorillas. Behavioral studies show that female mountain gorillas reach sexual maturity at age 6, followed by a 2 year period of sterility (Czekala and Sicotte, 2000). I would argue that sterility allows the body to fully develop and establish a baseline rate of sex hormone release needed for successful reproduction. Previous studies of sexual behavior and female hormones in gorillas reveal two phenomena: mating occurs during a brief mid-cycle period of maximal labial tumescence (swelling), and 17-β estradiol and testosterone reach peak concentrations during the same period (Nadler et al. 1983). These distinct hormonal peaks suggest that different aspects of sexual activity correspond with one or both of the two hormones (Nadler et al., 1983). However, only nulliparous females exhibit signs of estrous such as small labial swelling, but parous females do not (Czekala and Sicotte., 2000). Proceptivity of nulliparous females (pro-conception) is more variable compared to parous females that are proceptive for 1–4 days (Czekala and Sicotte, 2000). Czekala and Sicotte report the hormone pattern data for one individual female as the following: rising levels of estrogen 9 days prior to end of follicular phase, estrogen levels remain low during early to mid-luteal phase, then estrogen levels rise again by day 18. There was no clear pattern observed for progesterone (Czekala and Sicotte, 2000).

Labial swelling appeared to reach its maximum while estrogen levels were low, suggesting that estrogen does not play a prominent role in labial swelling of nulliparous female gorillas as it does in chimpanzees (Czekala and Sicotte, 2000). Though the levels of estrogen in both chimpanzees and gorillas differ drastically, higher levels in former and lower levels in the latter, estrogen is still necessary to facilitate the sexual swelling in gorillas. Comparison between chimpanzees and gorillas can highlight different aspects of the life evolutionary histories of each organism and help decipher what characteristics caused them to diverge from one another.

Sexual Swelling: White-handed gibbons

There appears to be a relationship between sexual swelling and mating systems: the absence of swelling has been observed in monogamous species and exaggerated swellings within polygamous species (Barelli et al., 2007). However, given that white-handed gibbons are monogamous, sexual swellings in gibbons are very perceptible. Gibbon swellings could most likely resemble that of polygamous practicing species (Barelli et al., 2007). Studies on captive white handed gibbons do not clarify the relationship between the sexual swelling cycle and ovulation or fertility phase, which is something that Barelli et al. sought to achieve (Barelli et al., 2007). Researchers measured levels of immunoreactive 5α-reduced 20 oxo pregnanes (5-P-3-OH) and fecal metabolites of progesterone (also known as progestogen) from fecal samples to determine the lengths of both the luteal and follicular phase of the menstrual cycle, as well as the possible day of ovulation and timing of the fertile phase (Barelli et al., 2007). Fecal progestogen was shown to have low levels in follicular phase, followed by elevated levels in the luteal phase (Barelli et al. 2007). Barelli et al. found that maximum swelling was limited to the follicular and early luteal phases, with a gradual decrease 4–5 days after post-ovulatory progestogen. Although maximum swelling duration varied between individuals, overall maximum swelling periods lasted 7–11 days (Barelli et al., 2007). Also, unlike other primate species age plays a role in the duration of the maximum swelling, the point at which swelling of perennial region is swollen to the highest degree, as older females have significantly shorter maximum swelling phases than younger females. Based on these results, younger female gibbons appear to have an advantage over older female gibbons, in that younger females have a longer period to find and attract mates. Even after fertilization, maximum swelling appeared at random intervals throughout pregnancies with average duration of 2.7 days (Barelli et al., 2007). These results suggest that maximum sexual swelling is not solely representative of ovulation and fertilization as it is in chimpanzees since swelling occurs throughout pregnancy in white-handed gibbons.

Social Hierarchy

Another reproductive characteristic of non-human primate species is social dominance of individuals by sex. Some species form social hierarchies among the males and/or females mainly because it reduces the amount of aggressive interactions year round as well as stress levels. Once social dominance is established, each individual peacefully complies with his or her societal role. However, one’s social status dictates their access to mates as well as their overall reproductive success, so those individuals with dominant status will benefit greatly. Evidence from various studies supports the hypothesis that higher ranked males experience greater reproductive success than subordinate males (Ellis, 1995). Dominant males obtain their high rank through aggressive behavior, which could be mediated by testosterone. However, the positive relationship between reproductive success and rank among females is not fully understood because some studies indicate the presence of a positive relationship, while others do not (Ellis, 1995). It seems that dominance would be associated with male reproductive success, as dominant males acquire more food and territory, rendering them more attractive than subordinate males to their female counterparts. Females are often attracted to males exhibiting high fitness, causing them to primarily reproduce with dominant males. There is a possibility that dominance may hinder male reproductive success in males due to the fact that dominant males spend so much time fighting to retain their dominant position while subordinate males use that time to reproduce instead. This tactic is referred to as a make-love-not-war effect (Ellis, 1995). Marmosets (Callithrix jacchus) and orangutans (Pongo pygmaeus) exhibit social dominance hierarchies, either male or female oriented, which influence the reproductive success of all individuals.

Social Hierarchy: Marmosets

The common marmosets are small-bodied, cooperatively breeding New World monkeys that live in multi-female social groups (Saltzman et al., 1998). The most dominant female within each group is the sole breeder since social status among females strongly regulates reproduction (Saltzman et al., 1998). Studies show that subordinate females fail to breed in both the wild and in captive groups instead, they aid the dominant female in providing care for her offspring (Saltzman et al., 1994). Subordinate females are also anovulatory (do not ovulate) due to a decrease in the pituitary release of the luteinizing hormone and the impaired secretion of the gonadotropin-releasing hormone (Saltzman et al., 1994). However, this hormonal suppression can be quickly reversed if a subordinate female is removed from the social group, showing elevated levels of plasma luteinizing hormone and ovulation within 2–3 weeks (Saltzman et al., 1994). Thus, the social status of female marmosets can change based on the social environment they are placed in, and with that change comes the possibility of breeding due to key alterations in hormone levels.

Researchers have shown that subordinate female marmosets have drastically lower plasma cortisol concentrations than dominant females, but it remains unclear whether the rank-related differences in plasma cortisol are a result of social status, drive it, or are the result of differences in reproductive function (Saltzman et al, 1998) (Saltzman et al, 1994). The Saltzman et al. (1994) study clarified the effects of social status, reproductive function and group formation on circulating levels of cortisol in adult female marmosets. The study included 32 captive-born adult female common marmosets that were pair-housed with adult males at least 12 days prior to the start of the experiment (Saltzman et al., 1994). The purpose was to determine the baseline cortisol level for each female for comparison in data analysis, and to ensure that all females began the experiment on the same level of cortisol. Females were placed in 1 of 8 different pre-assigned social groups, meaning all of them were exposed to the same “stimuli” per se (Saltzman et al., 1994). Social groups were formed by releasing 4 pre-assigned females and 4 adult males into a new home cage. Dominant status was assigned to females based on who the submissive behaviors were directed towards, and blood samples were collected to determine plasma cortisol levels that would support the researchers’ assumptions (Saltzman et al., 1994). Results showed that 15 females were cyclic (exhibit regular progesterone levels in both luteal and follicular stages), 8 females were oligocyclic (exhibit one or more luteal phase lasting less than 11 days and one or more follicular phase lasting more than 13 days), and 9 females as acyclic (exhibit no sustained elevation of progesterone concentrations above 10 ng/ml) prior to the formation of social groups (Saltzman et al., 1994). Results also showed that differences in cortisol levels did not become apparent until the second day of group formation: dominant females had significantly higher circulating cortisol levels than subordinate females (Saltzman et al., 1994). Researchers attribute this difference to wound formation from aggressive encounters because females who sustained wounds during group formation had significant elevation of cortisol over the basal level than those that refrained from wound aggression (Saltzman et al., 1994). Subordinate females that refrained from wound aggression did engage in high levels of agonism: they received

11 aggressive acts per hour from other females and performed

31 submissions per hour to other females (Saltzman et al., 1994). Subordinate females should logically exhibit higher levels of cortisol due to the stressful and aggressive encounters with other females, but the data shows that is not the case. The results from this study show that reproductive status was associated with plasma cortisol levels though, independent of social status, cortisol levels were substantially elevated in marmosets undergoing ovulatory females. Thus, high levels of cortisol relate to and/or possibly cause ovulation which subordinate females lack. Perhaps, low cortisol causes unsuccessful breeding in subordinates. This study shows how the privileged status of social dominance among female marmosets relate to reproductive advantages, which reveals how essential this reproductive behavior can be regarding reproductive success. This study could also shine light on the role of stress in women pregnancies and how the mother’s stress level can influence development of the fetus (Barbazanges et al, 1996).

Social Hierarchy: Orangutans

Male characteristics of the orangutan society include solitary nature, sexual dimorphism, and most importantly, the extended phase of sub-adulthood (Schurmann et al. 1986). Subadult males are physiologically mature, but lack the distinct features of dominant males like: big body, long hair, gular pouch, cheek callosities, and the inability to form the far-carrying long call (Schurmann et al. 1986). Orangutan groups are small, with the most common observed social unit consisting of a female and her offspring (Schurmann et al., 1986). However, consortship relationships have been observed and can include 2–8 individuals at a time that can remain together for months at a time (Schurmann et al., 1986). The males display one of the two sexually mature morphs: the prime flanged adult male or the unflanged subadult (Knott et al., 2010). Prime flanged males are dominant to unflanged males because they are significantly larger and exhibit the aforementioned secondary features (Knott et al., 2010). Unflanged males tend to use forced copulation more so than flanged males as an alternative mating behavior to resistance by females (Knott et al., 2010). The reproductive functioning of subadult males is not affected in any way because it has been reported that the reproductive system of young subadult orangutan males is successful as early as 8 years old (Schurmann et al., 1986). The breeding behavior of the orangutan male is divided into two parts. First, as a subadult he mates with as many females as possible to increase his chances of paternity for the next generation of offspring. Second, as a prime adult he consolidates and protects his contribution since consorting is fairly difficult due to his enormous size (Schurmann et al., 1986). Although it is unclear why some males develop before others, it is possible that stress can be a strong inhibitor of development, as glucocorticoids prevent the secretion of the growth hormone and the thyroid hormone (Thompson et al., 2012). A study conducted by Thompson et al. (2012) reports that male orangutans who completed their development before age 14 had higher testosterone levels than those that completed development after age 14. They found no significant variance in cortisol levels among the early and late maturing males as well as no correlation between cortisol levels and testosterone levels (Thompson et al., 2012). The authors concluded that early elevated levels of testosterone may play a beneficial role in the early transitional development from young subadult to prime flanged adult, while cortisol may not be associated with any aspect of this reproductive characteristic in male orangutans. A study conducted by Olweus et al. (1988) shows that the amount of circulating testosterone in adolescent human males does not necessarily deter their reproductive development, but does increase aggressive behavior.

Promiscuous Mating

Promiscuous mating has been observed in females of various species as a means of a reproductive behavior. Promiscuous mating is described as females mating with numerous males throughout the duration of their ovulatory cycle. This behavior helps reduce the chances of infanticide by other non-paternity males. Females who mate promiscuously can conceal ovulation from male counterparts. This reduces the likelihood of conception when an undesirable male forces copulation because they know the chance of conception is very low (Knott et al., 2010). This form of mating can be observed in both gorillas and orangutans.

Promiscuous Mating: Gorillas

Studies show that parous fertile female gorillas are proceptive for 1–4 days and the social groups in which they reside in often contain one male. About 40 percent of recorded social groups are multi-male, having more than one sexually active adult male (Stokes et al, 2003 Czekala and Sicote, 2000). Males who are able to mate with fertile females during that 1–4 day proceptivity period will have the best chance of reproductive success. According to Nadler et al (1983), males court females with soliciting, after which females “present”, meaning females willingly position themselves for mating after the male approaches her and pulls her towards him to cover her. Female success entails female solicitation followed by copulation with female solicitation referring to the female approaching the male followed by female presenting (Nadler et al., 1983).

Studies conducted by Nadler et al and Czekala and Sicotte report the role and function that principal hormones play in the physical display of labial swelling. Czekala and Sicotte’s study presents the first report of daily urinary hormone sampling in wild gorillas which combine mating observations and labial swelling (Nadler et al., 1983). Czekala and Sicotte found that mating and mating attempts occur at or near peak estrogen concentrations. Seven days after estrogen declines, progesterone increases, and both estrogen and progesterone increase at implantation (Czekala and Sicotte, 2000). Nadler et al. found that female solicited copulations occurred mainly outside the periovulatory phase, the period just before ovulation. Figure 1 shows that the hormone pattern during ovulation includes a midcycle preovulatory rise in estrogen, a smaller luteal phase peak, a midcycle peak of testosterone, and a luteal phase increase in testosterone (Nadler et al., 1983). Thirty-three percent of all copulations were initiated or female solicited, with 83 percent of these female solicited copulations occurring in the periovulatory phase (Nadler et al., 1983).

Figure 1: Top displays the days of copulation and hormone concentrations for five female gorillas, normalized to the day of the LH peak. Bottom displays both the perineal labial tumescence and hormone concentrations of a female gorilla during the menstrual cycle, normalized to the day of the LH peak (Nadler et al 1983).

Based on these results, with the data being normalized to the leutenizing hormone peak to determine the day of detumescence, the authors of this study came to the following conclusions concerning female gorillas: increases in copulation at midcycle are associated with midcycle concentrations of 17β-estradiol, the maximum frequency of copulations is associated with peak concentration of testosterone, and the absence of copulations during the mid-to-late luteal phase is associated with heightened levels of progesterone (Nadler et al., 1983). These results also suggest that females strategically mate with desirable males during their conception cycle or while ovulating (at estrogen peaks) which increases their chances of conception and implantation. Males tend to increase their likelihood of paternity through promiscuous mating, allowing their genes to be manifested in more offspring in the future generation due to multiple mating partners. Studies like these enhance our knowledge on what hormones are the principal roles during conception, which can than lead to more effective contraceptive agents for humans by targeting specific hormones and either suppressing or enhancing their secretion or activity.

Promiscuous Mating: Orangutans

Female orangutans show mating patterns modeling promiscuity as well. Promiscuous mating enables females the chance to allow direct or indirect manipulation of male mating access in accordance with fecundity or social context (Knott et al., 2010). In other words, males think females are not selective with regards to mating, but females tend to mate with their desirable partners while ovulating. Females also mate with non-dominant males to reduce the risk of infanticide by those males, but only during nonovulatory cycles will these matings occur (Knott et al., 2010). Female orangutans are subject to forced copulations by both dominant and subadult males on a regularly, but mostly by subadult males who feel the need to force themselves onto females as a counter strategy for not having dominant status (Barelli et al., 2007). Knott et al. (2009) observed when females resist aggressive behavior by either dominant or subadult males, the copulations do not last as long compared to willing copulations (Barelli et al., 2007). Dominant orangutan males indulged in forced copulations and overly aggressive behavior towards females more than subadult males. This complicates the notion that primary access to females for reproductive purposes is a benefit of garnering dominant status. However, prime males were reported to have obtained preferential mating access with the most fecund females (Knott et al., 2010).

Infanticide

Infanticide is considered to be a reproductive characteristic that is utilized by non-human primate species, chiefly males. For females, infanticide does not fully correspond with obtaining reproductive success since it entails the purposeful death of one’s offspring. Nevertheless, it occurs more so in non-human primate males because it allows the mother to be fertilized again soon afterwards (van Schaik et al, 1997). Animals perform infanticide for many reasons: exploitation, resource competition, parental manipulation and sexual selection (Cameron, 1996). Exploitation involves the death of offspring for the sole purpose of consumption or use of the victim (Cameron, 1996). Another reason why individuals would kill offspring is because the death of the infant would lead to increased access to resources for the killer and his or her descendants (Cameron, 1996). Parental manipulation involves the death of an infant by the parent(s) in order to improve the survival of the mother and existing offspring (Cameron, 1996). When resources are limited or in short supply, parents may be compelled to kill their younger offspring in order to provide for their older offspring who are closer to autonomy. Sexual selection, which entails competition between members of one sex (males) for reproductive investment by the other sex (females), may cause an animal (usually males) to kill another animal’s offspring (Cameron, 1996). For example, the offspring of female gorillas within a social group containing one alpha silverback male are at high risk once that alpha male dies because subadult males will attempt to fill that alpha male position. Once a new alpha male is in place, he will not want to care for another male’s young which leads him to kill the offspring of the females so that he can mate with them. He would then ensure that his legitimate offspring are reared and have access to the best resources. To prevent infanticide, female primates have utilized promiscuous mating because adult males would not know for certain the paternity of the offspring. Thus, it appears that promiscuous mating ensures the survival of one’s offspring by confusing paternity (van Schaik et al, 1997). Thus far, I have found no hormones associated with infanticide, though I would argue that testosterone levels would be higher in infanticidal males because they are trying to obtain a dominant status while securing resources for their future offspring, and dominant males have been found to have higher levels of testosterone (Anestis, 2006).

Costs and benefits of non-human primate usage for research

Strikingly similar attributes exist between humans and non-human primates, ranging from anatomy, physiology, and most importantly, endocrinology (King et al., 1988). These similarities make non-human primates an effective animal models for studies relating to immunology, pathology, reproductive biology, and more. Our common evolutionary ancestry has enabled certain processes to be conserved within humans and other primates, which suggests that processes within humans mirror those of other close related primates. Chimpanzees are one of the closest living relatives of humans (98% DNA match), which explains why they are the most widely used of the great apes (King et al., 1988). The most widely used lab animal nationwide are rodents, calculating

90% of usage in studies because they are so easy to manage, but incorporating non-human primates into research studies could help broaden our understanding of human biology, specifically reproduction. Currently,

30 primate species are being used in biomedical and behavioral research, with Old World species from Africa and Asia being among the most commonly used primates based on their ability to adapt to and reproduce well in captivity (King et al., 1988). Although primates are often the first choice of an investigator as an animal model, only

3.5% of the 20 million laboratory animals studied are primates due to several factors (King et al., 1988). The factors contributing to the restricted use of non-human primates include cost, limited supply, and appropriateness (King et al., 1988). It is relatively expensive to use non-human primates in research because most non-human primates are endangered from habitat loss caused by human activity (Shimizu et al., 2003). Since there is a restriction of non-human primate use, the studies that do request non-human primates must be suitable or deemed necessary because they are not needed for all studies (King et al., 1988). There are also regulations that must be followed to ensure that humane treatments of research animals are being upheld (King et al., 1988). Most primates in research are not allowed to be in terminal experiments, nor are they involved in studies that affect their breeding ability in any way, even though successful breeding programs are put in place to replenish the number of primates that do not survive in terminal experiments or just die from natural causes (King et al., 1988).

Despite the various similarities between humans and non-human primates which fuels the need to incorporate non-human primates in more research studies, we must be careful not to exploit and take advantage of these helpless animals. Though we as humans are dominant over non-human primates and other animals, we must not exacerbate the declining rates of endangered primates solely for further knowledge of our physiology. Thus, I argue that the incorporation of non-human primates into research studies should benefit in some way both parties: humans and non-human primates.

What We Can Learn About Ourselves?

Despite these restrictions on non-human primate use in research, there are numerous benefits that can be acquired from studies that used non-human primates. In some cases, the use of non-human primates are in dire need, like testing the efficacy and safety of treatments and vaccines that have been developed in studies using other animals as the animal model (King et al., 1988). Drugs that have been developed using rodents must be tested on closely related human relatives, like monkeys or chimpanzees, to get an idea of how efficient the drug will be if it is administered to humans. In other cases, non-human primates are the only viable option for the animal model when other species are not affected by or vulnerable to the disease under investigation (King et al., 1988). Ideally, an appropriate model organism is necessary to discover drugs that can combat human life-threatening diseases, like aids or cancer.

Studies on fertility control agents and the hormonal patterns involved in reproduction have gained valuable information on reproduction in both men and women due to the incorporation of non-human primates. Shetty et al. (1997) conducted a study to analyze the effects of estrogen deprivation in reproductive functioning of male and female primates using aromatase inhibitors. There are many estrogen dependent processes in female primates that occur throughout ovulation and non-ovulation cycles such as: the preparation of fallopian tubes for gamete interaction, early embryonic development, and preparation of the uterus for implantation (Shetty et al. 1997). Estrogen is therefore necessary in order to carry out the various processes that occur in female primate reproduction. Thus, the absence of such a vital component alters the functionality of these processes. The bonnet monkey was chosen as the primate model because past studies have shown its usefulness as a surrogate model for the human (Shetty et al. 1997). Shetty et al. (1997) found that estrogen deprivation led to the absence of preovulatory estrogen surge that normally occurs between days 8 and 11 in the female bonnet monkey. Estrogen deprivation affected the reproductive state of males as well, resulting in the enhanced secretion of the luteinizing hormone and testosterone which impairs reproduction (Shetty et al. 1997). This study was the first to use monkeys to test the efficacy of aromatase inhibitors as fertility regulator agents for men and women (Shetty et al. 1997). The conclusions they gathered could aid in developing aromatase inhibitors to induce super follicular maturation in women, as well as devising short term treatments to help increase testicular testosterone to boost spermatogenesis as a means of male fertility control (Shetty et al. 1997).

The use of non-human primate animal models will broaden our understanding of human biology and biological systems that cannot always be tested in humans. When it comes to reproduction, non-human primates are considered to be the closest model in relation to humans, which alludes to the reason why they are often sought after by many scientists. The endocrine mechanism of macaques has been investigated to analyze the role of prenatal hormone exposure in the determination of sexual phenotype (Shetty et al. 1997). Also, investigating the role of hormones in non-human primates like luteinizing hormone, testosterone, and follicle stimulating hormone that can be detected early in life, have shown that reversible elimination of elevated levels by treatment of GnRH agonists show that perinatal elevations of steroid hormones could alter normal sexual development in males particularly (Shetty et al. 1997).

What We Can Learn About Reproductive Systems in Primates

The involvement of non-human primates in research is and should not be one-sided, as in solely beneficial to humans advances in the reproductive capacity and fertility control can be made as well with the usage of non-human primates as animal models. For example, data has already been gathered on the influence of the CBC pill (combination birth control) on sexual behavior in women, but no data has been reported regarding its effects on gorilla estrous behavior. Safarty et al. (2012) examined the temporal trends of estrous, aggressive, affiliated, and activity budget data in a small group of 4 female gorillas while taking CBC pills. These CBC pills contain both synthetic estrogen and progestin followed by a week of placebo or sugar pills they suppress the activity of the HPG axis and instead promote follicle development, release and proliferation of uterine wall (Safarty et al., 2011). CBC is considered to be highly effective in lowland gorillas and is a popular choice of contraception throughout U.S. zoos for controlling reproduction (Safarty et al., 2011). The effects of CBC on other non-human primates have been documented already one of which shows that macaques behave more aggressively and that mating behavior in chimpanzees is reduced (Safarty et al., 2011). Desirable features of a contraceptive method include efficacy and having little to no effect on the social, sexual behavior of the animal. Compared to previous studies of uncontracepted gorillas that exhibited a peak of proceptive and receptive sexual behavior at time of ovulation (2nd week of menstrual cycle) which has also been observed in uncontracepted human females, the sexual behavior of contracepted gorillas in this study occurred in week 1 of menstrual cycle instead (Safarty et al., 2011). Also, 3 of the 4 female gorillas in this study showed aggressive behavior evenly throughout the cycle weeks (Safarty et al., 2011). This study shows that human based contraceptive methods such as CBC does not alter the endocrinology of female gorillas, but it does influence aggressive behavior as well as altered timing of sexual behaviors. Overall, human based methods can be administered to non-human primates specifically to aid in conservation efforts for breeding endangered non-human primate species, and still express the same level of efficacy.

The reproductive characteristics and behaviors of non-human primates vary between species and the presence and appropriate concentration of associated steroid hormones are vital to the efficacy of these mechanisms. The main hormones that drove the sexual swelling include estrogen and progesterone. The hormones associated with the social dominance hierarchies include cortisol and possibly elevated levels of testosterone, specifically in orangutans. Primate females that live in large social groups utilize promiscuous mating to combat the infanticidal incoming alpha males to save the lives of their children. Some primate species use more than one characteristic or behavior or a combination based on mating patterns or social hierarchy present within the species’ society. The various sex hormones involved in these characteristics and behaviors tend to be present at certain times (during ovulation or conception cycles), and at different concentrations to ensure correct functionality of the reproductive processes and to secure successful reproduction by producing offspring in the next generation. Since non-human primates share so many aspects of biology with humans due to common evolutionary ancestry, non-human primates are the most suitable model for developing safe breeding techniques for captive primate populations, as well as fertility agents for both men and women.

I would like to give a special thank you to the Barnard College Writing Center, my peers from the Fall 2014 Biology Senior Seminar course, and Professor Rebecca Calisi for taking out time to edit this semester-long project.


Footnotes

1 Assignment to the ‘pure-control’ and ‘romantic prime’ was randomized. The ‘active control’ was added at the request of a reviewer five months later. We did not initially include an ‘active control’ as: (1) results reported in [12] showed the effect of a ‘romantic prime’ is due to its content rather than the process of priming per se and (2) in a 3PPC game a pure-control is the standard control. As the results for the ‘active control’ and the ‘pure-control’ are the same (see electronic supplementary material, section B, table S1 and figure S1) we combined these. Furthermore, the demographics (1) age (F(2,82) = 0.621, p = 0.540) and (2) relationship status ( χ 2 2 = 0.878 , p = 0.654) did not vary across the three conditions.

2 Overall eight participants were paid. For the no-prime and romantic-primes conditions, which were run first, participants were told that five would be randomly selected. We later added the active-prime condition and in that we told participants that three would be selected at random.

Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4638143.

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

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Abstract

Explaining human evolution means developing hypotheses about the occurrence of sex differences in the brain. Neuroanatomy is significantly influenced by sexual selection, involving the cognitive domain through competition for mates and mate choice. Male neuroanatomy emphasizes subcortical brain areas and visual-spatial skills whereas that of females emphasizes the neocortex and social cognitive areas. In primate species with high degrees of male competition, areas of the brain dealing with aggression are emphasized. Females have higher mirror neuron activity scores than males. Hundreds of genes differ in expression profiles between males and females. Sexually selected differences in gene expression can produce neuroanatomical sex differences. A feedback system links genes, gene expression, hormones, morphology, social structure and behavior. Sex differences, often through female choice, can be rapidly modulated by socialization. Human evolution is a dramatic case of how a trend toward pair bonding and monogamy lowered male competition and increased female choice as a necessary step in releasing the cognitive potential of our species.


Genomic parasites (revisited)

Excerpt 1) “All placental mammals inherited their placenta from a single common ancestor that lived more than 100 million years ago,” he explained. “Whatever was happening then has long since been lost to history.”

My comment: That suggests whatever was happening in fish might be happening in mammals. Indeed, in a more recent news report, Victor Lynch claims to have found what was missing. “…we found the genetic changes that likely underlie the evolution of pregnancy are linked to domesticated transposable elements that invaded the genome in early mammals. So I guess we owe the evolution of pregnancy to what are effectively genomic parasites.”

What aspect of these genomic parasites explains their link to the evolution of pregnancy via links from a common ancestor? Was the common ancestor an egg-laying fish? If so, how are genomic parasites linked to sexual selection and placenta formation in fish?

Excerpt 2 from Biologists link sexual selection and placenta formation) “Describing the life histories of more than 150 species of fish in the family Poeciliidae, the researchers found that species with placentas tend to have males that do not have bright coloration, ornamentation or courtship displays. They tend to be much smaller than the males of species without placentas. They also tend to be very well endowed, enabling males to sneak up on females to mate with them without the formality of courtship.”

My comment: Did genomic parasites cause all of those differences some of them — any of them? Where’s the experimental evidence? Remember what Ellis and Silk (2014) said: “If there is none, it is not a scientific theory.”

Where did these genomic parasites come from? John Sedivy seems to be suggesting in this video (see 11:38 – 11:54) that the genomic parasites are “…molecular parasites that date back to the prebiotic dawn of time” (e.g., at the time when RNA was the first self-replicating molecule). See: Chromatin and epigenetic dynamics in senescence phenotypes – John Sedivy

That makes sense if the function of nutrient-dependent changes in the microRNA/messenger RNA balance link control of the DNA damage that transposons cause, via RNA-directed DNA methylation and RNA-mediated amino acid substitutions that link the pheromone-controlled physiology of reproduction to biodiversity in species from microbes to man. However, if the amino acid substitutions also lead to nutrient-dependent pheromone-controlled ecological adaptations, the theories of physicists and evolutionists are nothing more than pseudoscientific nonsense, which is what creationists believe.

If there is no scientific theory to support what you believe, the problem may be that you are a physicist or evolutionist. If what you observe about the obvious complexity of biodiversity is akin to what Darwin observed when he proposed that ‘conditions of life’ must be considered before natural selection or sexual selection are relevant, you may be a creationist, like Dobzhasky, who wrote: “…the so-called alpha chains of hemoglobin have identical sequences of amino acids in man and the chimpanzee, but they differ in a single amino acid (out of 141) in the gorilla.” — in Nothing in Biology Makes Any Sense Except in the Light of Evolution

If he were not still dead, I’m rather certain he would by now have realized that amino acid substitutions differentiate all cells of all individuals of all species and mutations cause physiopathology. See also: Combating Evolution to Fight Disease. Unfortunately, others still don’t know the difference between an amino acid substitution and a mutation. See, for example:

Excerpt: “After years of looking for mutations that cause diseases, investigators are now searching for those that prevent them.”

My comment: Mutations cause diseases, fixed amino acid substitutions prevent them. See instead:

Excerpt: “This regulatory change thus alters EDA expression at the same body site where freshwater fish lack body armor, while preserving important functions of EDA in other tissues. These results provide a new example of a specific regulatory change linked to morphological evolution in natural populations (Martin and Orgogozo 2013), and add to growing evidence that regulatory changes are a predominant mechanism underlying adaptive evolution in sticklebacks (Jones et al. 2012) and other organisms (Wray 2007, Carroll 2008).”

My comment: A mutation links the lack of body armor in fish from the FGFR3 to more than 99 percent of cases of human achondroplasia, which is a form of short-limbed dwarfism. “Specifically, the protein building block (amino acid) glycine is replaced with the amino acid arginine at protein position 380 (written as Gly380Arg or G380R). Researchers believe that this genetic change causes the receptor to be overly active, which leads to the disturbances in bone growth that occur in this disorder.” FGFR3

Mutated FGFR3 genes also are linked to a variety of other diseases and disorders. “Among 62 human cases of seborrheic keratosis (182000), Logie et al. (2005) found that 39% of samples harbored somatic activating FGFR3 mutations, identical to those associated with skeletal dysplasia syndromes and bladder and cervical neoplasms (see, e.g., 134934.0005 and 134934.0013). Logie et al. (2005) implicated FGFR3 activation as a major cause of benign epidermal tumors in humans.” FIBROBLAST GROWTH FACTOR RECEPTOR 3 FGFR3

Why haven’t others learned the difference between fixed amino acid substitutions that stabilize the DNA in organized genomes and mutations? The answer to that question takes us back to what’s known about physics. For example, extended discussion of Atoms can be in two places at the same time led to this claim:

I wrote: “Mutagenesis experiments take meaningless results and meaningfully interpret them. Most people are intelligent enough to know that — even if they are, like you, biologically uninformed.

Andrew Jones responded with a link to a 2001 publication: How so? The basic idea of them is introducing random changes to enzymes and observing their effects.

Mutagenesis (link opens pdf)They bring it up in that paper and I’ve brought it up before- if mutations can never be beneficial, then the SOS response wouldn’t exist.

My comment: He linked to a 2001 paper that claims: “…the increased expression of a number of genes whose products not only assist the cell to survive DNA damage but also increase mutation rates (Friedberg et al., 1995 Frank et al., 1996, and see below).”

Our 1996 review Hormones and Behavior review links RNA-mediated cell type differentiation from species of microbes to man via the conserved molecular mechanisms of what is now known to be the biophysically constrained chemistry of protein folding by amino acid substitutions, which is what I detailed in my 2013 review with examples of cause and effect across species. Nutrient-dependent/pheromone-controlled adaptive evolution: a model. Andrew Jones is more than a decade behind the experimental evidence I used to support my model.

“…many of these nutrients have a clear link to brain health, including omega-3s, B vitamins (particularly folate and B12), choline, iron, zinc, magnesium, S-adenosyl methionine (SAMe), vitamin D, and amino acids.”

What’s not clear is how researchers can continue to ignore the obvious fact that nutrient-dependent RNA-directed DNA methylation links RNA-mediated events from quantum physics to quantum biology and behavior via amino acid substitutions that differentiate the cell types of all cells in all individuals of all species during their development.

Again, see my model: Nutrient-dependent/pheromone-controlled adaptive evolution: a model. There is no excuse for anyone willing to learn to not realize that “If you learnt evolutionary biology and genetics a decade or more ago you need to be aware that those debates have moved on very considerably, as has the experimental and field work on which they are based.” (p. 1014) — Neo-Darwinism, the Modern Synthesis and selfish genes: are they of use in physiology?

About James V. Kohl

James V. Kohl was the first to accurately conceptualize human pheromones, and began presenting his findings to the scientific community in 1992. He continues to present to, and publish for, diverse scientific and lay audiences, while constantly monitoring the scientific presses for new information that is relevant to the development of his initial and ongoing conceptualization of human pheromones.