Human Sperm Competition
KeywordsSperm Competition Seminal Fluid Cervical Mucus Fertile Phase Female Orgasm
Human Sperm Competition
The competition to fertilize a woman’s egg between sperm from two or more different men.
Sperm competition was first studied in insects (Parker 1970), but was soon suspected to occur in other animals, including humans (Smith 1984). A series of publications (see Robin Baker and Mark Bellis: Pioneers of Research on Human Sperm Competition) claimed to have found evidence that confirmed this suspicion. These claims triggered a wave of opposition (see Opposition to human sperm competition).
Currently, authors are divided into three main groups. The first (e.g., Baker and Bellis 1995; Gallup et al. 2006) considers that sperm competition occurred sufficiently often in the human past to have been a major selective pressure on sexuality. The second (e.g., Dixson 2009; Larmuseau et al. 2016) proposes that human sperm competition happened rarely and has played either a minor or zero role in human evolution. The third (Marczyk and Shackelford 2010) maintains that the actual frequency does not matter. As long as sperm competition occurs with some predictability and carries large fitness costs, even a relatively low frequency can act as a powerful selective pressure.
For the moment this debate continues unresolved. Alongside this discussion, however, aspects of human behavior, psychology, physiology, and anatomy are being demonstrated that seem to make sense only as adaptations to sperm competition (Shackelford et al. 2016). A brief summary follows, divided into three sections. The first considers when, where, and how sperm might compete, and the next two consider the potential evolutionary impact of such competition on first male and then female sexuality.
Competing Sperm: When, Where, and How
The following descriptions are based on the review and extensive references in Baker and Bellis (1995).
A man stores sperm in two long narrow tubes in his lower abdomen. Each tube (vas deferens) extends from a testis to the single prostate gland. Inside this gland, the two tubes join the urethra (the duct that runs the length of the penis). While in the vas deferens sperm are highly concentrated in just a small amount of fluid from the testis. The maximum number of sperm stored in the two tubes at any one time is ~1000 million with older sperm nearer the penis and younger sperm nearer the testes.
A woman’s unstretched vagina is more a slit than a tube. Protruding into the upper vagina is the cervix (the lower part of the uterus). The cervical opening ranges in shape from a circular dimple to a transverse slit. Inside the cervix the walls are lightly adpressed on a column of mucus that moves forever downward in glacier-like fashion eventually to drip into the upper vagina.
When copulation begins, the penis distends the vagina, everywhere touching the internal walls. Just before ejaculation a portion of each of the two “columns” of sperm is shunted from the vas deferens into the urethra. Ejaculation then follows. The upper part of the vagina dilates like a balloon, in effect creating a bowl to receive the semen.
While contractile waves force the sperm from the urethra, secretions from first the prostate then the seminal vesicles add volume. On average, ~300 million sperm in ~3 ml of semen are ejaculated in a series of 3–9 spurts, often with a copulatory thrust between each spurt. The result is an inseminate that for two reasons is neither homogenous nor all in one place. First, the seminal fluids differ chemically between spurts. The first part is dominated by prostate gland secretions and the later parts by fluids from the seminal vesicles. The very last spurt is strongly spermicidal. Secondly, the spurts are inseminated with different force by a penis that may change in length and turgor from first spurt to last. The end product is a “seminal pool” next to the cervical opening, plus semen from later spurts and dribbles lower down the vagina.
It is not known what happens on the, presumed infrequent, occasions that a woman is inseminated by two males simultaneously nor how the two ejaculates and contained sperm might interact if she does.
Immediately after, or even during, insemination, the cervix dips into the seminal pool, creating a cervical mucus-semen interface. Virtually simultaneously, most of the ejaculate, excluding the part nearest the cervical opening, coagulates to form a soft, gel-like structure which does not become liquid again for 15–20 minutes. Coagulation retains the seminal pool in position while sperm leave to cross the cervical mucus-semen interface.
After the seminal pool decoagulates, the upper vagina contains a mixture of the now-liquid-again seminal fluid, various female secretions, and stranded sperm. If the cervix dips again into this mixture, such as during female orgasm, more sperm can still escape into the cervix. If not, no more sperm can leave the pool. Eventually, the female ejects the whole mixture from the vagina as the “flowback.”
The flowback exits the vagina as a discrete series of 3–7 white globules and measures ~3 ml; in effect the female rids her vaginal tract of virtually all of the seminal fluid plus any sperm still contained. This event occurs between 15 and 120 min after the male ejaculated (0–105 min after the seminal pool decoagulates). If expelled during urination, the flowback is sometimes ejected with surprising force.
All flowbacks contain sperm, on average ~35% of the number inseminated (range: 5% to ~100%).
Only when a woman mates with a second male before ejecting the flowback from the first male do two ejaculates interact inside a vagina. In the UK, ~1% of women with >500 lifetime copulations claimed at some time to have been inseminated by two different males within <30 min (Baker and Bellis 1995). In the USA, ~8% of college undergraduate women claim to have engaged in group sex (1 woman, 2 or more men) at least once (Gallup et al. 2006). On most such occasions, the second male will remove the first male’s ejaculate with his penis (see section on ‘Penis shape and copulatory behavior’ below) before himself ejaculating. If he does not, however, the two ejaculates interact in the vagina.
There are two phases and elements to this interaction. First, for ~15–20 minutes after the first male ejaculated, his coagulated seminal mass can function as a short-term plug, a physical barrier that keeps sperm from the second ejaculate away from the cervix. Secondly, after decoagulation, the spermicidal back part of the ejaculate from the first male could decrease the motility and survival of sperm in the second male’s ejaculate. Counteracting this, however, the prostatic first half of the second male’s ejaculate provides some protection to its contained sperm.
Cervical mucus has a complex structure with fibrils arranged to form channels. Sperm migrate through the mucus by way of these channels. There are two channel arrangements within a cervix: vertical, aligned more or less parallel to the cervical walls, and diagonal, running from the lower (vaginal) end of the mucus column to crypts in the cervical wall. Compared with a sperm, which is ~3 μm wide, the vertical channels are spacious (30–35 μm), whereas those through the diagonal mucus are relatively narrow (2–6 μm). Proportions of the two types vary over time with vertical channels dominating during the fertile phase of the menstrual cycle.
The dipping of the cervix into the seminal pool allows sperm to escape from the vagina. The mucus-semen interface consists of a series of finger-like projections of semen extending a short way into the mucus channels. Once across the interface, sperm then swim either through the vertical mucus, perhaps directly to the uterus, or along the diagonal channels into the cervical crypts.
Around 65% of sperm from an inseminate successfully enter the cervical mucus, but the vast majority then go no further. Within minutes of first sperm entry, the female floods the mucus with white blood cells (leucocytes). These attack the invaders, killing and removing them by phagocytosis, targeting healthy sperm just as aggressively as the dead, and dying. At their peak, a few hours after insemination, leucocytes may outnumber sperm by up to 3:1. Within 24 hours of insemination, however, leucocyte numbers have returned to base level.
Only ~1% of sperm (~3 million) from the inseminate successfully evade the leucocytes. Some that do so pass straight through into the uterus, but the vast majority instead find safe haven in one of the 10,000 or so crypts that dot the cervical walls. While in these crypts, safe from phagocytosis, the sperm become immotile until expelled. Expulsion occurs suddenly but is staggered over days with a peak 24 hours after insemination.
Most (~99%) sperm that enter the cervical mucus never leave alive, reaching neither the uterus nor the crypts. Instead, they are either intercepted by leucocytes or simply lodge in the mucus. Even these sperm, however, can play a part in sperm competition. By blocking channels through the cervical mucus and attracting leucocytes, they can greatly hinder the passage of sperm from any second male that inseminates the female over the next day or so.
Competition can also occur in and around the cervical crypts. As sperm from a second male attempt to enter and settle in these crypts, then later jostle after expulsion, the presence of sperm from a previous male can interfere with both maneuvers.
Except when pregnant, a woman’s uterus (womb) is roughly pear sized as well as pear shaped with the walls pressed closely together. Vanguard sperm that swam straight through the vertical channels of the cervical mucus arrive within 5 minutes of insemination. These are then helped to the womb’s top, the widest part of the pear. In effect, they surfboard, carried on the crests of muscular ripples passing up the walls. At the top of the womb on each side, where horns would be if the “pear” was a bull’s face, is an opening (the uterotubal) leading into a narrow tube, the oviduct. Once through the opening, the sperm swim a short distance along the oviduct until reaching a rest area (the isthmus). Here most cease swimming, settle down, and wait.
The wave of sperm that passes through the uterus just minutes after insemination is neither the largest nor the last. Numbers in the uterus peak ~24 hours after insemination as further sperm arrive following expulsion from the cervical crypts.
The uterus seems merely a zone that sperm must traverse to reach the oviduct. As it is possible to arrive in the oviduct too soon as well as too late, sperm from two or more men are not really “racing” during the traverse. Only if early sperm can hinder later sperm in some way (e.g., by blocking the uterotubal junction or occupying better positions in the oviduct), does there seem scope for competition during this leg of the journey.
Fertilization occurs in the ampulla, the region of the oviduct furthest from the uterus. Beyond the ampulla is an opening into the female’s body cavity near one of the two ovaries. Roughly every 2 months, a particular oviduct receives an egg, which then remains fertile for only ~24 hours.
Only ~25,000 sperm from an inseminate of ~300 million ever pass through an oviduct. At any one time only ~3500 are present and of these only ~300 are in the ampulla. Most often, after several hours residing in the isthmus, sperm set off individually to swim to and through the ampulla then on into the body cavity where they die. However, on those rare occasions that an egg is released by the nearby ovary, a chemical “signal” arrives, and many sperm from the isthmus swim to the ampulla simultaneously. Whether an egg arrives or not, 4–5 days after a single insemination, there are no sperm left in the oviduct.
A sperm’s timing of arrival at the ampulla may be more important than speed. However, when an “egg-approaching” signal is given, the swim from isthmus to ampulla might become a race.
A single insemination is most likely to lead to fertilization if it occurs 48 hours before ovulation, which is roughly the time taken for the sperm population to peak in the oviduct. However, not all sperm even in the oviduct are able to fertilize an egg: only 1 in 7 have such ability (compared with an even lower 1 in 300 in the original inseminate). This means that of the ~25,000 sperm that pass through the oviduct, only about ~4000 are capable of fertilization, and of the 300 found at any one time in the ampulla, only ~40.
It is generally assumed that when sperm from two or more males compete inside a female, the male who has most sperm in the ampulla as the egg arrives has the greatest chance of fertilization. Whether the critical factor is “most sperm” or “most sperm capable of fertilizing an egg” is not yet clear. Much depends on the function, if any, of the 86% (6/7) in the oviduct not capable of fertilization. Two explanations have been offered: (1) that these sperm are faulty, hence irrelevant, and (2) that they hinder, divert, or even kill fertile sperm from rival males.
Selection on Men
Human males, whether paired to women monogynously (1:1, male/female) or polygynously (1:>1, male/female), invest significant time, energy, and “wealth” into raising their partners’ children. Evolutionarily, a male gains most if these children are his own genetic offspring (Trivers 1972). Sperm competition, due to a partner’s infidelity, threatens a male’s reproductive success because it raises the possibility of cuckoldry, leading a male unknowingly to expend resources on raising another man’s child. Selection, therefore, favors a man who either prevents sperm competition or, if he fails, ‘wins’ the competition that ensues.
Pham and Shackelford (2014) contrast the “risk” and “intensity” of sperm competition: risk refers to the likelihood that the male’s sperm will face competition, while intensity refers to the number of males that contribute sperm to that competition. Shackelford (2003) proposes that human males encounter three separate adaptive problems from sperm competition: anticipation, prevention, and correction. The first two are generated by risk and lead to adaptations that motivate mate choice and guarding. The last is generated by intensity and leads to adaptations such as copulatory behavior, genital morphology, ejaculate qualities, and the number and behavior of sperm. Some behaviors, such as routine sex, are adaptations to all three problems.
Anticipation: Mate Choice
Males who choose more-faithful long-term partners are less likely to encounter sperm competition, and evolution should favor men who can reliably identify such women.
Men show agreement on which women are likely to be unfaithful, their judgment seemingly based on female attractiveness. There is also some evidence that this judgment has foundation. Women with features shown to be attractive to men (e.g., low waist-to-hip ratio, bilateral symmetry, and feminine voices) have been reported to accumulate more sexual partners, including committing more acts of infidelity (Baker 1997; Hughes et al. 2004; Shackelford and Buss 1997; but see Rhodes et al. 2005).
Prevention: Mate Guarding
Once committed to a relationship, a man shows some ability to judge his partner’s faithfulness (Andrews et al. 2008), in part by analyzing her behavior (Shackelford and Buss 1997). He can also assess to a degree whether any child she bears is likely to be his genetic offspring (Anderson 2006).
Buss (1988) identified 19 male tactics that reduce sperm competition including surveillance, threatening rival men, and direct guarding (i.e., spending as much time with the partner as possible). Such guarding succeeds: in the UK the more time a man spends with his partner between copulations, the less likely she is to be unfaithful (Baker and Bellis 1995). A man can also recruit other family members to keep surveillance on his partner in his absence (Strassmann et al. 2012).
Some men attempt to enforce fidelity through violence and in places have their actions supported by law. The earliest known example, from 4300 years ago, is found in the Mesopotamian Code of Urukagina (French 2008) which advocated stoning unfaithful women to death. A number of modern societies still allow a death sentence for females accused of infidelity.
Despite men’s attempts to prevent partner infidelity, they do from time to time fail. Estimates of the proportion of children sired by a man other than their putative father range from ~10% (Baker and Bellis 1995; Anderson 2006) to ~1% (Larmuseau et al. 2016) (see Opposition to human sperm competition). Perhaps in consequence, men also show adaptations that seem to increase their chance of “winning” any sperm competition that results.
Men seem motivated to maintain a population of sperm inside their partners, and the greater the risk of sperm competition, the larger the population maintained (Baker and Bellis 1995). This adaptation anticipates partner infidelity, guards against another male’s sperm having uncontested access to the partner’s egg, and provides some chance of correcting the female’s infidelity by still being the male to fertilize her egg.
The strategy a man is suggested to use (Baker and Bellis 1995) is to maintain reservoirs of sperm in his partner’s cervical crypts, thereby ensuring a continuous passage of fresh sperm through her oviducts for up to ~5 days after each insemination. Intercourse at least every 5 days is sufficient, combined with varying the number of sperm inseminated according to time since last copulation.
Over a period of 4 weeks, the total number of sperm inseminated into a partner averages about 3000 million and varies little whether the couple have sex 20, 10, or 5 times in that period (Baker and Bellis 1995). However, if the man spends less time physically “guarding” his partner between copulations and the risk of sperm competition increases, the total number of sperm he inseminates also increases (Baker 1997).
A recent (<72 hours) masturbation reduces the number of sperm inseminated at the next copulation but not the number that enter the cervix (Baker 1997). Such masturbatory “shedding” may increase inseminate competitiveness by removing older sperm. Thus, at the next copulation, the male inseminates younger sperm which could survive longer inside the female. Potentially, masturbation is an adaptation to sperm competition.
Response to Sight of a Copulating Pair
Males of many species respond to perception of a copulating pair by attempting either to oust and take over from the other male or, failing that, to mate with the female as quickly thereafter as possible (review: Baker and Bellis 1995). To achieve this, perception of a copulating couple needs to generate a rapid arousal for copulation and the sperm competition that inevitably follows. In male humans the appeal of hard-core pornography rests on such a response. Surveys have shown that men prefer images of a woman with multiple men, suggesting sperm competition, compared to those of a man with multiple women (McKibbin et al. 2013).
Urgent and/or Forced “In-Pair” Copulation
Just as with directly observed infidelity, a man who strongly suspects his partner of recent infidelity increases his chances of avoiding being cuckolded by inseminating her himself as soon as he can. This is especially the case if he suspects the infidelity to be very recent (<2 hours). Until the flowback from the previous male is ejected, that male’s sperm can still be entering the cervix (Baker and Bellis 1995).
Men who spend a greater percentage of time absent from a partner report greater sexual interest in that partner, greater distress in response to sexual rejection, and a greater sexual persistence if rejected (Shackelford et al. 2007). This increased drive to inseminate a partner suspected of infidelity can lead to force being used (Wilson and Daly 1992): most forced within-pair copulations follow accusations of female infidelity.
Penis Shape and Copulatory Behavior
Until ejected in the flowback, one male’s semen can hinder any second male’s sperm trying to enter the cervix, but this earlier semen can be removed.
The erect human penis is piston shaped with a smooth terminal protuberance (= coronal glans). This shape, the fit of the penis in the vagina, and the pumping/thrusting action during copulation together mean that as a penis pushes forward then pulls back, semen already present is sucked down the vagina. On the next forward thrust, the glans pushes through this material; then on the next backward pull, the back edge of the glans scrapes the material further down the vagina in a “push-pull-suck-push-pull-scrape” process (Baker and Bellis 1995). This process has been verified by Gallup et al. (2003) using artificial penes, vaginae, and semen. Gallup et al. also reported that after a perceived female infidelity or period of female absence, males thrust deeper, faster, and more vigorously.
Males of primates with high levels of sperm competition have proportionately larger testes (relative to body size) than males of species with low levels (Harcourt et al. 1995). Larger testes produce more sperm at a faster rate. Evolutionarily, in lineages with greater sperm competition, the organs increase in size until the gain from greater competitive success is opposed by some other factor (e.g., cost of maintaining larger testes, or greater risk of damage). Relative testes size for humans is ~4 times greater than for gorillas (with low sperm competition) but ~5 times smaller than for Chimpanzees (with high). This suggests an evolutionary past for humans with intermediate levels of sperm competition.
Testes size varies greatly within populations. Baker and Bellis (1995) hypothesized that men with larger testes are specialized for sperm competition and men with smaller testes for mate guarding. Between the two extremes, men follow a mixed strategy. In support of this hypothesis, men with larger testes: (1) spend less time with their established partner (Baker and Bellis 1995), (2) show less interest in their partner’s children (Mascaro et al. 2013), (3) copulate and ejaculate more frequently (Baker and Bellis 1995), (4) inseminate more sperm at each copulation (Baker 1997), (5) ejaculate more sperm during masturbation (Baker 1997; Simmons et al. 2004), and (6) are more likely to become involved in sperm competition (Baker 1997; Baker and Bellis 1995; but see Simmons et al. 2004).
Human ejaculates contain a proportion (up to 40%) of strangely shaped sperm. Head shape, for example, can be small, large, pear shaped, cigar shaped, or simply oddly shaped. Tails vary too: short, bent, coiled, or double. Traditionally, such sperm have been blamed on mistakes during sperm formation (Cohen 1977). However, Baker and Bellis (1988) suggested that they were adaptations to sperm competition, some even present specifically to die, a “kamikaze” role (see: Robin Baker and Mark Bellis: Pioneers of Research on Human Sperm Competition.)
Selection on Women
Most discussion surrounding sperm competition focuses on males, but females also gain benefits (Smith 1984). If sperm competitiveness is heritable, females fertilized by the most competitive sperm will gain through the greater reproductive success of their sons. To obtain this advantage, a female needs to promote sperm competition via double mating (matings that lead to the presence of sperm from two or more males inside her reproductive tract) at around the time of peak fertility.
Weak Signals of Fertility
To double-mate a female must, at key moments, evade mate guarding by her established partner. Several adaptations have evolved to make such evasion easier (review: Welling and Puts 2015).
Female humans are sexually receptive both throughout the menstrual cycle and during pregnancy. This background receptivity makes it more difficult for male partners to identify the critical days to guard the female intensively. Nevertheless, females do not, and maybe cannot, hide their fertile phase completely.
“Oestrous” is the phase of the female cycle leading up to and just following ovulation. During this phase a suite of attributes appear, all of which are less pronounced at other times. In humans, not only do females travel further and show more interest in mating with multiple males at this time (Baker and Bellis 1995), but also they advertise their phase of cycle through subtle changes in appearance, behavior, attitude, sound, and smell (review: Welling and Puts 2015).
How effectively men can detect and act upon the oestrous signals given by women is still debated, but clearly they cannot interpret the signs with total certainty (see Welling and Puts 2015). For example, men of the agricultural Dogon tribe of Mali forced their wives to advertise menses by temporarily residing in special “menstrual” huts. When menstruation finishes, the wives are then for a while kept under intense surveillance by their husband’s family network. Consequently, the number of Dogon children fathered by a man other than a woman’s husband was low (Strassmann et al. 2012). However, when a section of the population relaxed its use of the menstrual hut, the frequency of such “extra-pair” paternities increased fivefold, suggesting that direct detection of the fertile phase by males was weak at best.
Timing of Double Mating by Women
Nationwide data for women in the United Kingdom revealed that general female infidelity showed no pattern with respect to the menstrual cycle (Baker and Bellis 1995). However, double matings “unprotected” by contraception were most likely to occur during the fertile phase, suggesting that the women were most likely to promote sperm competition when the probability of conception was highest (see Robin Baker and Mark Bellis: Pioneers of Research on Human Sperm Competition for more details).
Cryptic Female Choice
Women use a range of information when choosing long- and short-term partners (Shackelford et al. 2016; Welling and Puts 2015) and make comparisons between the two when promoting competition between their sperm. Females also have a variety of adaptations that allow them to bias the chances of fertilization in favor of a particular male.
Although such “favoritism” is not shown by younger nulliparous women, it is shown by women in the main reproductive phase of their lives (Baker 1997). The latter are less likely to use contraception during sex with a male who is not their established partner. They also, by altering the occurrence and timing of their orgasms, seem to retain more sperm from this other male than from their partner.
For further details of this function of the female orgasm plus opposition to the findings, see Robin Baker and Mark Bellis: Pioneers of Research on Human Sperm Competition; for a general review of the female orgasm, see Puts et al. (2012).
Debate continues over whether sperm competition occurred often enough in the past to play a significant part in the shaping of human sexuality. Yet at the same time a body of work is amassing, covering many aspects of human behavior, psychology, physiology, and anatomy, that seems to make sense only in terms of adaptation to sperm competition.
Human sperm have a long and complex journey ahead of them when they are first inseminated into a vagina, and most falter within minutes or hours. An average of ~35% never escape the vagina and <1% ever get further than the neck of the womb (the cervix). Each leg of the journey raises its own unique circumstances and, when sperm from more than one male are present, raises different types of opportunity for those sperm to meet, interact, and compete.
The threat of sperm competition appears to have imposed a range of selective pressures on men. Advantages can be gained from preventing such competition, but when preventive measures fail, the only adaptive avenue is to try to win the sperm competition that then ensues. Sexual psychology, mate choice, mate guarding, masturbation, copulatory behavior, ejaculate size, penis shape, testes size, and sperm morphology have all been argued to have been shaped by sperm competition.
The evolutionary impact of sperm competition is not limited to males. Females would also appear to gain by promoting such bouts. Various behaviors and attributes may all have evolved to aid such promotion; So, too, may responses such as sperm ejection and orgasm (female) that could influence the outcome of any sperm competition the female generates.
If the opposition to the role of sperm competition is justified, then all of these apparent adaptations will need to be explained in other ways. However, if sperm competition has indeed been the force that many scientists claim, it has been a highly significant factor in the shaping of human sexuality.
- Andrews, P. W., Gangestad, S. W., Miller, G. F., Haselton, M. G., Thornhill, R., & Neale, M. C. (2008). Sex differences in detecting sexual infidelity—Results of a maximum likelihood method for analyzing the sensitivity of sex differences to underreporting. Human Nature: An Interdisciplinary Biosocial Perspective, 19, 347–373.CrossRefGoogle Scholar
- Baker, R. R., & Bellis, M. A. (1995). Human sperm competition: Copulation, masturbation and infidelity. London: Chapman and Hall.Google Scholar
- Cohen, J. (1977). Reproduction. London: Butterworths.Google Scholar
- Dixson, A. F. (2009). Sexual selection and the origins of human mating systems. Oxford: Oxford University Press.Google Scholar
- French, M. (2008). From Eve to Dawn: A history of women in the world, Origins: From prehistory to the First Millennium (Vol. I). New York: The Feminist Press at CUNY.Google Scholar
- Marczyk, J.B., & Shackelford, T.K. (2010). A biased, incomplete perspective on the evolution of human mating systems. A review of Alan F. Dixson (2009), Sexual selection and the origins of human mating systems. Evolutionary Psychology, 8, 31–36.Google Scholar
- Shackelford, T. K. (2003). Preventing, correcting and anticipating female infidelity. Evolution and Cognition, 9, 90–96.Google Scholar
- Shackelford, T. K., Goetz, A. T., McKibbin, W. F., & Starratt, V. G. (2007). Absence makes the adaptations grow fonder: Proportion of time apart from partner, male sexual psychology, and sperm competition in humans (Homo sapiens). Journal of Comparative Psychology, 121, 214–220.CrossRefPubMedGoogle Scholar
- Shackelford, T. K., Goetz, A. T., LaMunyon, C. W., Pham, M. N., & Pound, N. (2016). Human sperm competition. In D. M. Buss (Ed.), The handbook of evolutionary psychology, Foundations (Vol. 1, 2nd ed., pp. 427–443). Hoboken: Wiley.Google Scholar
- Trivers, R. L. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 139–179). London: Aldine Publishing Co..Google Scholar
- Welling, L. L. M., & Puts, D. A. (2015). Female adaptations to ovulation. In V. A. Weekes-Shackelford & T. K. Shackelford (Eds.), Evolutionary perspectives on human sexual psychology and behavior (pp. 243–260). New York: Springer.Google Scholar
- Wilson, M., & Daly, M. (1992). The man who mistook his wife for a chattel. In J. H. Barkow, L. Cosmides, & J. Tooby (Eds.), The adapted mind (pp. 289–322). New York: Oxford University Press.Google Scholar