Benenson, Webb, and Wrangham note that sexual selection explains many traits of human males and suggest that “no unifying theory explains traits expressed more in females.” They therefore propose a generalized version of Campbell's “staying alive” hypothesis: Human females evolved unique, self-protective survival adaptations driven by the importance of maternal and grandmaternal care. Benenson et al. review evidence in support of this hypothesis, including evidence that females live longer and show less risk-taking behaviors, greater avoidance of interpersonal conflicts, lower pain thresholds, more effective immune responses, and more frequent sleep disturbances.
We agree that theory and data suggest that human females exhibit stronger self-protective reactions than males do, and that these reactions were likely adaptive for ancestral females. These ideas indeed help unify our understanding of some female adaptations – though not others, such as fat deposition on the breasts, hips, and buttocks, which are putative sexually selected female ornaments that may be costly to survival (Pawłowski & Żelaźniewicz, Reference Pawłowski and Żelaźniewicz2021), and maternal investment through gestation and lactation, which deplete energy reserves and decrease longevity (Wood, Reference Wood2017). Here, we make two additional points to advance this discussion.
First, there is a more general theory that links a broader set of human female traits: Females are the more “ecological sex” (Gaulin & Sailer, Reference Gaulin and Sailer1985). While sexual selection favors traits that aid in mating competition, ecological selection favors traits for other functions, including survival, fecundity, and offspring survival. Gaulin and Sailer (Reference Gaulin and Sailer1985) provided evidence that nutritional factors influence the evolution of primate body size, but males deviate further from the ecologically optimum size in species in which they compete more intensely for mates. Gaulin and Sailer (Reference Gaulin and Sailer1985) note that the hypothesis that females tend to be more ecologically optimized “is a very general one. The idea that the precision of ecological adaptation will vary with both sex and mating system suggests a functional perspective from which any morphological, physiological, or behavioral pattern of sex differences might be studied” (p. 117). The hypothesis that females, more than males, possess self-protective adaptations thus accords well with the more general hypothesis that females are relatively optimized under ecological selection compared to males in species in which males experience stronger sexual selection.
Second, more evidence is needed to make a strong case that specialized survival adaptations evolved in human females. Such adaptations may instead have been selected in both sexes, with a lower level of expression favored in males due to tradeoffs with traits favored in mating competition, and many survival adaptations are likely to be ancestral and not human specializations. Benenson et al. state that “it is not simply degree of mate competition that produces sex differences in self-protectiveness,” but the problem with inferring otherwise from the evidence reviewed by Benenson et al. is that this evidence consists of human sex differences in various traits, and sex differences can result from adaptations in either sex. Without additional evidence, a sex difference in the degree of mating competition remains the more parsimonious explanation.
For example, Benenson et al. claim that greater female longevity is an evolutionary response to women's larger role in childcare, but cross-species data are needed to pull apart contributions of female parental investment from male sexual selection. In all mammals, females engage in greater parental investment, but males outlive females in approximately 40% of wild mammal populations (Lemaître et al., Reference Lemaître, Ronget, Tidière, Allainé, Berger, Cohas and Gaillard2020). Sex differences in longevity appear to relate more consistently with the intensity of sexual selection in males (Tidière et al., Reference Tidière, Gaillard, Müller, Lackey, Gimenez, Clauss and Lemaître2015), which may lead to male phenotypes that are more susceptible to environmental threats (Lemaître et al., Reference Lemaître, Ronget, Tidière, Allainé, Berger, Cohas and Gaillard2020). Human sex differences in mortality due to homicide, suicide, and accidents are also highest in young adulthood when male mating competition is most vigorous (Wilson & Daly, Reference Wilson and Daly1985).
Reduced female risk-taking and same-sex aggression are shared with humans' close living relatives (Harrison, Noble, & Jennions, Reference Harrison, Noble and Jennions2021; Rohner, Reference Rohner1976), and sex differences in these traits were likely present in the common ancestor of the great apes because risk-taking and aggression increased male mating success and the expense of survival (Archer, Reference Archer2009; Carter & Kushnick, Reference Carter and Kushnick2018; Flinn, Ponzi, & Muehlenbein, Reference Flinn, Ponzi and Muehlenbein2012; Kruger, Wang, & Wilke, Reference Kruger, Wang and Wilke2007; Luoto & Varella, Reference Luoto and Varella2021; Muñoz-Reyes et al., Reference Muñoz-Reyes, Polo, Valenzuela, Pavez, Ramírez-Herrera, Figueroa and Pita2020; Puts, Carrier, & Rogers, Reference Puts, Carrier, Rogers, Buss and Durkeein press). Decreased responses to pain and decreased pain sensitivity in males may also reflect an evolutionary history of male–male mating competition (Archer, Reference Archer2019; Puts et al., Reference Puts, Carrier, Rogers, Buss and Durkeein press; Vigil et al., Reference Vigil, Rowell, Chouteau, Chavez, Jaramillo, Neal and Waid2013), and susceptibility to infectious disease may be a costly side-effect of the development of sexually selected male traits (Folstad & Karter, Reference Folstad and Karter1992; Moore & Wilson, Reference Moore and Wilson2002).
Benenson et al. propose that sex differences in nighttime awakenings and disturbances reflect heightened vigilance to physical and social threats among women. However, mating competition has also likely shaped patterns of sleep sacrifice (Faria, Varela, & Gardner, Reference Faria, Varela and Gardner2019), and when sleep sacrifice is used to protect the group against threats during nighttime, evolutionary theoretical models predict that females should sleep more, not less, than men (Faria et al., Reference Faria, Varela and Gardner2019). Some evidence indicates that women sleep longer than men (Burgard & Ailshire, Reference Burgard and Ailshire2013) and have better sleep quality (Faria et al., Reference Faria, Varela and Gardner2019). In BaYaka foragers (Kilius et al., Reference Kilius, Samson, Lew-Levy, Sarma, Patel, Ouamba and Boyette2021), males displayed a higher variance in sleep patterns and spent more time socializing during nighttime.
Relatively stronger ecological selection may indeed have shaped specialized survival adaptations in human females (Campbell, Reference Campbell2010; Stockley & Campbell, Reference Stockley and Campbell2013), but further evidence is needed to make a compelling case. Are these putative survival adaptations more prevalent in primate species in which females invest more in offspring, controlling for levels of male mating competition? Are some unique to human females? Many traits in human males, such as muscularity, low voice pitch, and facial hair, emerge at puberty when male mating competition intensifies (Aung & Puts, Reference Aung and Puts2020; Puts, Reference Puts2016). Do some putative female survival adaptations emerge across pregnancy or parturition, after female mating competition becomes less exigent in relation to the importance of surviving to care for offspring? We look forward to learning more.
Benenson, Webb, and Wrangham note that sexual selection explains many traits of human males and suggest that “no unifying theory explains traits expressed more in females.” They therefore propose a generalized version of Campbell's “staying alive” hypothesis: Human females evolved unique, self-protective survival adaptations driven by the importance of maternal and grandmaternal care. Benenson et al. review evidence in support of this hypothesis, including evidence that females live longer and show less risk-taking behaviors, greater avoidance of interpersonal conflicts, lower pain thresholds, more effective immune responses, and more frequent sleep disturbances.
We agree that theory and data suggest that human females exhibit stronger self-protective reactions than males do, and that these reactions were likely adaptive for ancestral females. These ideas indeed help unify our understanding of some female adaptations – though not others, such as fat deposition on the breasts, hips, and buttocks, which are putative sexually selected female ornaments that may be costly to survival (Pawłowski & Żelaźniewicz, Reference Pawłowski and Żelaźniewicz2021), and maternal investment through gestation and lactation, which deplete energy reserves and decrease longevity (Wood, Reference Wood2017). Here, we make two additional points to advance this discussion.
First, there is a more general theory that links a broader set of human female traits: Females are the more “ecological sex” (Gaulin & Sailer, Reference Gaulin and Sailer1985). While sexual selection favors traits that aid in mating competition, ecological selection favors traits for other functions, including survival, fecundity, and offspring survival. Gaulin and Sailer (Reference Gaulin and Sailer1985) provided evidence that nutritional factors influence the evolution of primate body size, but males deviate further from the ecologically optimum size in species in which they compete more intensely for mates. Gaulin and Sailer (Reference Gaulin and Sailer1985) note that the hypothesis that females tend to be more ecologically optimized “is a very general one. The idea that the precision of ecological adaptation will vary with both sex and mating system suggests a functional perspective from which any morphological, physiological, or behavioral pattern of sex differences might be studied” (p. 117). The hypothesis that females, more than males, possess self-protective adaptations thus accords well with the more general hypothesis that females are relatively optimized under ecological selection compared to males in species in which males experience stronger sexual selection.
Second, more evidence is needed to make a strong case that specialized survival adaptations evolved in human females. Such adaptations may instead have been selected in both sexes, with a lower level of expression favored in males due to tradeoffs with traits favored in mating competition, and many survival adaptations are likely to be ancestral and not human specializations. Benenson et al. state that “it is not simply degree of mate competition that produces sex differences in self-protectiveness,” but the problem with inferring otherwise from the evidence reviewed by Benenson et al. is that this evidence consists of human sex differences in various traits, and sex differences can result from adaptations in either sex. Without additional evidence, a sex difference in the degree of mating competition remains the more parsimonious explanation.
For example, Benenson et al. claim that greater female longevity is an evolutionary response to women's larger role in childcare, but cross-species data are needed to pull apart contributions of female parental investment from male sexual selection. In all mammals, females engage in greater parental investment, but males outlive females in approximately 40% of wild mammal populations (Lemaître et al., Reference Lemaître, Ronget, Tidière, Allainé, Berger, Cohas and Gaillard2020). Sex differences in longevity appear to relate more consistently with the intensity of sexual selection in males (Tidière et al., Reference Tidière, Gaillard, Müller, Lackey, Gimenez, Clauss and Lemaître2015), which may lead to male phenotypes that are more susceptible to environmental threats (Lemaître et al., Reference Lemaître, Ronget, Tidière, Allainé, Berger, Cohas and Gaillard2020). Human sex differences in mortality due to homicide, suicide, and accidents are also highest in young adulthood when male mating competition is most vigorous (Wilson & Daly, Reference Wilson and Daly1985).
Reduced female risk-taking and same-sex aggression are shared with humans' close living relatives (Harrison, Noble, & Jennions, Reference Harrison, Noble and Jennions2021; Rohner, Reference Rohner1976), and sex differences in these traits were likely present in the common ancestor of the great apes because risk-taking and aggression increased male mating success and the expense of survival (Archer, Reference Archer2009; Carter & Kushnick, Reference Carter and Kushnick2018; Flinn, Ponzi, & Muehlenbein, Reference Flinn, Ponzi and Muehlenbein2012; Kruger, Wang, & Wilke, Reference Kruger, Wang and Wilke2007; Luoto & Varella, Reference Luoto and Varella2021; Muñoz-Reyes et al., Reference Muñoz-Reyes, Polo, Valenzuela, Pavez, Ramírez-Herrera, Figueroa and Pita2020; Puts, Carrier, & Rogers, Reference Puts, Carrier, Rogers, Buss and Durkeein press). Decreased responses to pain and decreased pain sensitivity in males may also reflect an evolutionary history of male–male mating competition (Archer, Reference Archer2019; Puts et al., Reference Puts, Carrier, Rogers, Buss and Durkeein press; Vigil et al., Reference Vigil, Rowell, Chouteau, Chavez, Jaramillo, Neal and Waid2013), and susceptibility to infectious disease may be a costly side-effect of the development of sexually selected male traits (Folstad & Karter, Reference Folstad and Karter1992; Moore & Wilson, Reference Moore and Wilson2002).
Benenson et al. propose that sex differences in nighttime awakenings and disturbances reflect heightened vigilance to physical and social threats among women. However, mating competition has also likely shaped patterns of sleep sacrifice (Faria, Varela, & Gardner, Reference Faria, Varela and Gardner2019), and when sleep sacrifice is used to protect the group against threats during nighttime, evolutionary theoretical models predict that females should sleep more, not less, than men (Faria et al., Reference Faria, Varela and Gardner2019). Some evidence indicates that women sleep longer than men (Burgard & Ailshire, Reference Burgard and Ailshire2013) and have better sleep quality (Faria et al., Reference Faria, Varela and Gardner2019). In BaYaka foragers (Kilius et al., Reference Kilius, Samson, Lew-Levy, Sarma, Patel, Ouamba and Boyette2021), males displayed a higher variance in sleep patterns and spent more time socializing during nighttime.
Relatively stronger ecological selection may indeed have shaped specialized survival adaptations in human females (Campbell, Reference Campbell2010; Stockley & Campbell, Reference Stockley and Campbell2013), but further evidence is needed to make a compelling case. Are these putative survival adaptations more prevalent in primate species in which females invest more in offspring, controlling for levels of male mating competition? Are some unique to human females? Many traits in human males, such as muscularity, low voice pitch, and facial hair, emerge at puberty when male mating competition intensifies (Aung & Puts, Reference Aung and Puts2020; Puts, Reference Puts2016). Do some putative female survival adaptations emerge across pregnancy or parturition, after female mating competition becomes less exigent in relation to the importance of surviving to care for offspring? We look forward to learning more.
Conflict of interest
None.