Extended female sexuality
Extended female sexuality is where the female of a species
Although this behaviour incurs costs to females, such as energy and time,[2] many researchers have proposed reasons for its existence. These hypotheses include the male assistance hypothesis, which proposes that females gain non-genetic benefits (such as food and shelter) in exchange for sexual access.[1] A sub-hypothesis of this is Hrdy's, proposing extended female sexuality as an adaptive process aiming to creating paternity confusion in males.[6][7] Alternative hypotheses, classified as 'male-driven', claim that extended female sexuality occurs due to male adaptations, resulting from an inability to detect fertility status in females or to dampen immune responses against sperm.[1][8][9] Finally, Spuhler's hypothesis suggests that the behaviour may have arisen as an incidental effect of larger adrenal glands in humans.[1]
Occurrence
In non-humans
Although not found in all organisms, researchers have identified sexual intercourse patterns in certain animals that reflect extended female sexuality, such as in some old world primates, birds and insects.
In humans
Human females are considered to exhibit the greatest degree of extended female sexuality, with receptivity to sexual intercourse remaining constant across fertile and infertile phases of the reproductive cycle, including during pregnancy, lactation, and in adolescence. In a study of 20,000 women from 13 countries, frequency of copulation was reportedly the same across all stages of the ovarian cycle. The only notable drop in sexual behaviour occurred during menstruation. Therefore, women largely showed the same level of sexual behaviour in the non-fertile phases of their ovarian cycles as in the fertile phases.[5][16]
Researchers have investigated the effect of hormonal contraceptive use in women on the frequency of sexual intercourse.[17] Many of these contraceptives mimic a pregnancy state in females by altering hormone levels. Therefore, women who use these contraceptives do not experience the fertile phases of their cycles. In a systematic review, it appeared that the frequency of sexual intercourse was unaffected by contraceptive use in the majority of women. Although artificially created, this adds to the literature documenting the existence of copulation in humans during non-fertile periods.[18]
Impact of concealed ovulation
In order to encourage
Explanations
Male assistance hypothesis
Mating outside the fertile window of their ovarian cycle may incur considerable costs for females, such as in time and energy usage. To counteract these costs, the male assistance hypothesis argues that females exhibit extended sexuality to obtain resources from males.[22][23] These resources vary between species, but can include food, social alliance, and protection of the female and her offspring.[2] For example, in the Trobriand tribe, men give women gifts in exchange for sexual access.[24] From this hypothesis, three predictions can be made.[1]
Male provision of non-genetic resources
Firstly, in species that demonstrate extended female sexuality, there should be evidence that the males provide non-genetic resources to females. This prediction is supported in a variety of animals,[25] with reviews revealing that male assistance (such as food or protection), is provided to certain mammals and communally breeding birds in exchange for mating outside the conceptive period.[26] For example, female blackbirds that solicit mating outside the fertile period have increased mate guarding from their pair-bonded partner. This increases protection against other sexually coercive males and ensures the provision of other material benefits.[19][27] In a review investigating primates that exhibit extended female sexuality, it was noted that females engaging in extended sexuality benefited from increased offspring protection and paternal care from males.[28][29]
Enhanced reproductive success
Secondly, in order to outweigh the aforementioned costs, mating during infertile phases should increase females' reproductive success by increasing the number of offspring produced. Current research has only investigated this factor indirectly, and it has predominantly been investigated in insects. For example, when male insects deliver material benefits in exchange for sexual access, the reproductive success of the females increases with the number of matings.[1][30] It is important to note that the mating behaviour assessed was not limited to extended female sexuality. Hence, it only provides indirect support for the second prediction.
Shifting mate preferences and behaviour across the ovarian cycle
The final prediction of the male-assistance hypothesis has been extensively investigated. It predicts that females will exhibit differing mate preferences during fertile and non-fertile periods. Specifically, when fertile, the females will be sensitive to indicators of high genetic quality to increase the genetic quality of her offspring.[5] Conversely, outside of the fertile period, females will show a preference for males who can provide resources for her and her offspring. In most species, males of higher genetic quality offer fewer non-genetic resources (such as shelter and food) than those of lower quality, so females are likely to choose different males at each stage.[1]
Evidence for this prediction has been found in many different species. In
In addition to impacting mating preferences, females have been found to exhibit differing mating behaviour at different cycle stages. An analysis of 121 studies with female birds showed that most mate outside their pair bond at a higher rate when fertile, especially when the primary partner possesses indicators of low quality genes. During infertile phases, birds showed reductions in this behaviour, suggesting that the function of extended female sexuality is not to increase the genetic quality of offspring.[35] In humans, females show increased motivation for mating with other males at mid-cycle without an accompanying increase in copulation with their long-term partner, especially if the partner was less physically attractive.[5]
Hrdy's hypothesis
Hrdy's hypothesis is an extension of the male assistance hypothesis, in that both hypotheses argue that women have evolved this adaptation to gain some tangible benefit from males. According to Hrdy's hypothesis,[6][7] extended female sexuality is an adaptive process with an aim of creating paternity confusion in their male counterparts.[1] Paternity confusion refers to the male being unsure as to whether offspring are genetically his own. If the female mates with different males (at all points of her ovarian cycle) whilst concealing fertility, then the males will inevitably have paternity confusion.
Paternity confusion is proposed to be an adaptive function for preventing infanticide.[36][37][38] Thus, if the female can successfully create paternity confusion, males will be less likely to kill her offspring, as the lack of paternity certainty means that they run the risk of killing their own genetic offspring. Additionally, the males, in turn, are likely to protect the same female's offspring from infanticide that may be committed by other adults within the species. Once again, this is because they are uncertain about paternity, and aim to protect infants that are genetically their own.
Paternity confusion in primates
Researchers have analysed the behaviour of
Criticism of Hrdy's hypothesis emerges from evidence which suggests that male primates can discriminate between their own offspring and the offspring of others.[40][41] In one study, researchers analysed the DNA of 75 juvenile baboons to conclude who fathered them. They found that males selectively cared for their own offspring, particularly when their offspring became involved in aggressive confrontations which posed the possibility of injuries or a threat to their social standing. Evidently, if males can discriminate between their own offspring and the offspring of others, then there is no purpose in the female attempting to create paternity confusion during the pregnancy stage. This would be counter-intuitive, as, once the offspring is born, the males will know whether the offspring is, or is not, their own. Future research will need to be conducted in this vein to investigate whether males in other species show the ability to discriminate between their own offspring and the offspring of others before coming to any decisive conclusions.
Concealed estrus as a function of paternity confusion in primates
Research is fairly consistent in the finding that species with concealed estrus mate at all stages of their ovarian cycle. For instance, mating activity in
Hrdy's hypothesis has been criticised, however, on the basis that some female primates show both extended female sexuality and sexual swellings.[1] In terms of Hrdy's hypothesis, these two concepts are incompatible. Sexual swellings appear only during the most fertile phase of the female's ovarian cycle, with the purpose of advertising fertility. In sharp contrast, according to Hrdy, extended sexuality is adapted to conceal fertility and ensure mating across all stages of the ovarian cycle, to aid paternity confusion.
Male-driven hypotheses
One of the alternative explanations is that extended female sexuality is 'male-driven'. This hypothesis is theoretically based on male uncertainty regarding the fertility status of females.[1] Although some physiological changes occur during the fertile period that may act as reliable indicators (e.g. the concentration of oestrogen can change female scent), most species have not evolved signals advertising fertility (e.g. sexual swellings).[43] Therefore, males will be unable to detect fertility with any precision. As a result, extended female sexuality is proposed as a male sexually selected trait. Males will pursue sexual access throughout the entirety of the ovarian cycle to increase their chances of impregnating the female. According to this hypothesis, females lack any benefit from this activity due to their inability to conceive, yet will be coerced by males to engage in sexual intercourse.[44]
The training hypothesis
Another hypothesis claiming that extended female sexuality has evolved to benefit males' interests is the 'training hypothesis'. It has been shown that women's
This hypothesis has received much criticism [citation needed]. For example, as all mammals experience the same immune system responses to sperm antigens, this hypothesis predicts that all mammals should exhibit extended female sexuality. However, only few species of mammals exhibit sexual behaviour outside the conceptive period.[47] On the other hand, eclampsia is virtually unique to humans and thus the Training Hypothesis may only be relevant to extended female sexuality in humans.[48]
Spuhler's hypothesis
Spuhler's hypothesis is a stand-alone hypothesis of extended female sexuality. Spuhler suggests that extended female sexuality has evolved as a by-product of an adaptation in females that increases the levels of
See also
References
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- ^ Engelhardt, Antje (2004). The Significance of Male and Female Reproductive Strategies for Male Reproductive Success in Wild Longtailed Macaques (Macaca Fascicularis). Göttingen: Cuvillier Verlag. p. 3.
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Further reading
- Buss, D. M. (2015). The Handbook of Evolutionary Psychology, Foundation (Chapter 13). New York: John Wiley & Sons.
- Campbell, L. (2009, June 17). Comparison of the sexuality of humans, common chimpanzees and bonobos.
- Shackelford, T. K., & Hansen, R. D. (2015). The Evolution of Sexuality (Chapter 8). New York: Springer.
- Simpson, J. A., & Campbell, L. (2013). The Oxford Handbook of Close Relationships (Chapter 17). Oxford: University Press.
- Thornhill, R., & Gangestad, S. W. (2008). The Evolutionary Biology of Human Female Sexuality (Chapter 3). Oxford: University Press.