Male Reproductive Variance
Within species or breeding population variation in male reproductive success.
Within a species, individuals vary in reproductive success. In a sexual reproducing species, where each individual has one male and one female parent, increased reproductive success for certain individuals of one sex necessitates decreased reproductive success for others of that sex. Put more directly, the more extreme the winners, the more extreme the losers. While the focus of this entry is male reproductive variance, it will by necessity to also discuss female reproductive variance as a contrast, as reproductive variance is a major factor both of and contributing to sex differences, which coevolve with both mating strategies and parental care.
Coevolution with Parental Investment/Care
Across species, males tend to show greater variance in reproductive success than females. This results from females typically having a lower potential reproductive rate relative to males; a fundamental difference is rooted in anisogamy – differential investment in gametes by males versus females, the basis of sexual reproduction. Parental investment is defined as investment in one offspring (or current offspring) to the exclusion of other (particularly future) offspring (Trivers 1972). Because energetic and time investments in particular offspring come at the cost of investing in different behaviors or young, exclusionary efforts toward any particular reproductive event comes at the cost of continued investment in past reproduction, or investment in potential future reproduction.
Even if the only parental investment in a species is initial gamete production, females are obligated to a higher per-offspring investment than males, and this initial difference in investment is thought to the ultimate basis of the general tendency toward females having higher parental investment than males (Trivers 1972). This difference can be more profound in species such as mammals where females have obligate parental investment far beyond gamete production. Looking at humans as a sample mammal, the maximum recorded number of putative offspring for a man is ~888 (Oberzaucher and Grammer 2014), 12.9 times the maximum of 69 recorded for a women (in 27 pregnancies, all births were multiples; Guinness World Records 2016). The fact that females tend to be the “slower” sex – that is, requiring more “time-out” between or resource input into reproductive events – has the consequence of their typically being the limiting sex. Therefore, males, as the usually more reproductively available sex, are faced with a higher likelihood of being excluded from reproduction (as above, because every offspring has one-and-only-one male and female genetic parent), resulting in male variability in reproductive success being typically higher than that in females (known as Bateman’s principle; Bateman 1948).
This difference in reproductive success variation tends to result in males being relatively more competitive for access to mates (females being a limiting resource for reproduction; Trivers 1972) and females being relatively more choosy about potential mates. It should be noted that this does not exclude the possibility that both sexes are both competitive and choosy – there is no expectation that males mate indiscriminately nor that females do not vie for the more valuable (in terms of direct resources or good genes) males. Rather, it means that on average, males will be more engaging in intrasexual competition over mates than females, and females will be more choosy over mates than males.
Coevolution with Mating Systems
Generally speaking, the degree of variation in reproductive success within a sex is closely tied to the species-typical mating system (Davies et al. 2012). For examples, in species where the typical mode is monogamy, both males and females show relatively low reproductive variance, particularly in comparison with systems where females (polyandrous), males (polygynous), or both sexes (promiscuous) have simultaneous multiple mates. However, even in monogamous systems, there is room for variation (e.g., Brown et al. 2009). For example, individuals may differ in their likelihood of ever entering a partnership (e.g., particularly if there is a biased sex ratio), and the number of lifetime partnerships may differ between individuals (and also between the sexes).
Among humans, cultural variation in “exclusive sexual partnerships” or marriage practices is associated with the reproductive variance in the sexes in those cultures. In relatively few cultures, women are exclusively sexual with multiple men (in several of these examples, these men are related to one another), but men “officially” have sexual access only with her. These cultures are often ones where the “cost” of obtaining a wife is high, or there are few available women due to some other cultural or life-history factor (Starkweather and Hames 2012).
More frequently documented are polygynous cultures, where one man monopolizes sexual access to multiple women (this may be associated with strict control of women to prevent her having sex with other men; Chamberlin and Guiora 2014). Such societies often have associated with them reproductive control or expulsion of other men (typically subordinates, sometimes involving castration of non-evicted men; Chamberlin and Guiora 2014). However, not all polygynous cultures have such high male skew, and societies noted as polygynous may express a more mild form of occasional polygyny in the context of overall monogamy or increased re-pairing by men relative to women (e.g., Brown et al. 2009). In fact, many cultures identified as monogamous may be better, from a behavioral ecology perspective, be labelled as mildly polygynous, particularly due to the commonality of serial monogamy.
Complicating matters is the fact that studies frequently show that men on average report a higher number of sexual partners than women; while this likely results in part from opposing cultural pressures that drive men to overreport and women to underreport their number of partners, other factors (such as access to sex workers, who are not subsequently surveyed) can help explain this discrepancy. Overall, humans appear to, on average, broadly fit a pattern of moderate polygyny, and male reproductive variance is typically higher than that of females (e.g., Hammer et al. 2008), although as above, this is rather variable, and unlike many animal species, it is difficult to identify a clearly “typical” human mating system, as there is considerable variation of form even within these broad categories (see discussion in Brown et al. 2009).
Consequences of Variation in Male Reproductive Success
Sexual selection influences the degree of reproductive variance observed within the sexes, and evolution of mating strategies in response to differential reproductive success further propagates sexual selection. The effects of male reproductive variance on mating systems have resulted in myriad complicated expressions of male reproductive behavior, and differential reproductive success among males is often associated with variation (either discrete or continuous) in other aspects of their morphology and reproductive behavior (e.g., Davies et al. 2012). Note that similar variation between sexes within a species (sexual dimorphism), though not invariably the result of sexual selection, can also be rooted in a difference in reproductive success variation between males and females (Davies et al. 2012). For example, if certain traits permit males access to mates through mate preference or through competition, those traits will tend to evolve to become sexually dimorphic (for an extreme example, consider the anglerfish, where females are up to half a million times heavier than males, who become functionally parasitic on the female they adhere to; Pietsch 2005).
The most striking examples of reproductive success coevolving with male reproductive phenotype can be observed in nonhuman animal species where males show profound within-species variation in individual morphology and reproductive behavior. These reproductive phenotypes may represent different life-history pathways (e.g., Ruffs, where alternative types also have a genetic basis; Lank et al. 1995), or different life stages (e.g., orangutans; Knott 2009), with the result males may or may not exhibit multiple reproductive phenotypes in their lifetime. Among fishes, males in species with alternative male tactics may display clearly discrete morphological and behavioral phenotypes, to the extreme that males of the same species may appear to the naïve observer to be different species (see Taborsky 1994 for an overview of alternative reproductive tactics among fishes). Certain avian species and mammalian species also show similar, though often less profound, discrete variation in male reproductive phenotype (e.g., Leboeuf 1972; Lank et al. 1995; Knott 2009). Typically, alternative phenotypes are associated with different levels of reproductive success, although the strategy with the highest lifetime reproductive success is not necessarily always those large showy dominant males (e.g., Berejikian et al. 2010).
More typically, differences in male reproductive success are correlated with continuous male trait variation of traits involved in mate attraction or intrasexual competition (see overview in Davies et al. 2012). Such traits may be associated with ability to sequester resources (e.g., energetic reserves or mating resources such as territories), attract mates (e.g., by signaling genetic quality, compatibility, or ability to provide direct benefits to offspring), or outcompete other males for mating access (e.g., traits that enhance strength or stealth). Males who possess traits that allow increased control of reproductive resources and potential males have increased individual reproductive success.
From a comparative perspective, the phenotypic variation seen among human males in likely response to reproductive success variation is relatively muted. Data are restricted as there are relatively few studies of human reproduction that directly assess offspring number and outcome; far more frequently examined is mating success or partnership formation. That said, some male traits have been shown to be predictive of reproductive success, both production and survival of offspring, with the caveat that putative offspring are not necessarily fathered by that man, and males may underreport offspring resulting from women they do not have an official partnership with. Relationships are typically in the continuous fashion described above, although it is not always a linear correlation. These traits include voice pitch (Apicella et al. 2007); performance in ritual fights (Llaurens et al. 2009); physical traits such as height (average or moderately tall being most successful; Nettle 2002; Stulp et al. 2012), weight (Schooling et al. 2011), BMI (Sear 2006), and upper-body strength (Apicella 2014); hunting ability (Kaplan and Hill 1985; Smith 2004); personality (Alvergne et al. 2010); and wealth/higher socioeconomic status (Nettle and Pollet 2008). Also, as males with higher reproductive success are typically judged as more physically attractive (e.g., Jokela 2009), we can expect that some factors correlated with perceived attractiveness should also predict reproductive success. Additional traits that would be expected to correlate with traits above have been shown to be predictive of mating success, and it is therefore reasonable to presume that they are also likely predictive of reproductive success.
Reproductive variance coevolves with parental investment and mating system and influences and is influenced by sexual selection pressures. The initial bias of increased parental investment by females relative to males is related to the typical cross-taxa finding of greater reproductive variance among males than among females. Degree of variation within and between the sexes is tied to mating, and there is a feedback loop between the forces and consequences of sexual selection resulting from male reproductive variation. In nonhuman animals, the consequences of reproductive variance among males can be extreme variation in reproductive phenotype (both morphology and behavior). Similar variation related to reproductive success can be observed in a less elaborate and typically more continuous fashion among human males.
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