Exposure to female olfactory cues hastens reproductive ageing and increases mortality when mating in male mice.

Theories of ageing predict that investment in reproduction will trade-off against survival and later-life reproduction. Recent evidence from invertebrates suggests that just perceiving cues of a potential mate's presence can reduce lifespan, particularly in males, and that activation of neuroendocrine reward pathways associated with mating can alleviate these effects. Whether similar effects occur in vertebrates remains untested. We tested whether exposure to olfactory cues from the opposite sex would influence mortality and reproductive senescence in male mice. We observed that males exposed to female olfactory cues from middle- to old age (from 10 to 24 months of age) showed reduced late-life fertility, irrespective of whether they had also been allowed to mate with females earlier in life. Males that were exposed to female odours in conjunction with mating also showed an increased mortality rate across the exposure period, indicating that olfactory cues from females can increase male mortality in some environments. Our results show that exposure to female odours can influence reproductive ageing and mortality in male mice, highlighting that sensory perception of mates may be an important driver of life-history trade-offs in mammals.

Mating in the absence of fertilization promotes a growth-reproduction versus lifespan trade-off in female mice.

Trade-offs between growth, reproduction, and lifespan constrain animal life histories, leading to evolutionary diversification of life history cycles in different environments. In female mammals, gestation and lactation are expected to impose the major costs of reproduction, driving reproductive trade-offs, although mating also requires interactions with males that could themselves influence life history. Here we show that a male's presence by itself leads to lifelong alterations in life history in female mice. Housing C57BL/6J female mice with sterilized males early in life led to an increase in body weight, an effect that persisted across life even when females were later allowed to produce pups. We found that those females previously housed with sterile males also showed enhanced late-life offspring production when allowed to reproduce, indicating that earlier mating can influence subsequent fecundity. This effect was the opposite to that seen in females previously housed with intact males, which showed the expected trade-off between early-life and late-life reproduction. However, housing with a sterile male early in life came at a cost to lifespan, which was observed in the absence of females ever undergoing fertilization. Endocrinologically, mating also permanently reduced the concentration of circulating prolactin, a pituitary hormone influencing maternal care. Changes in hormone axes that influence reproduction could therefore help alter life history allocation in response to opposite-sex stimuli. Our results demonstrate that mating itself can increase growth and subsequent fecundity in mammals, and that responses to sexual stimuli could account for some lifespan trade-offs normally attributed to pregnancy and lactation.

Incel Activity on Social Media Linked to Local Mating Ecology.

Young men with few prospects of attracting a mate have historically threatened the internal peace and stability of societies. In some contemporary societies, such involuntary celibate-or incel-men promote much online misogyny and perpetrate real-world violence. We tested the prediction that online incel activity arises via local real-world mating-market forces that affect relationship formation. From a database of 4 billion Twitter posts (2012-2018), we geolocated 321 million tweets to 582 commuting zones in the continental United States, of which 3,649 tweets used words peculiar to incels and 3,745 were about incels. We show that such tweets arise disproportionately within places where mating competition among men is likely to be high because of male-biased sex ratios, few single women, high income inequality, and small gender gaps in income. Our results suggest a role for social media in monitoring and mitigating factors that lead young men toward antisocial behavior in real-world societies.

Widespread Promiscuity and Cheap Weddings: Can "Low-Value" Sexual Relationships Make Certain Individuals More Sexually Conservative?

Attitudes toward sexual relationships can have evolutionary underpinnings because these attitudes often serve, or at least reflect, the attitude holder's mating self-interest. Sexually restricted individuals, for example, hold conservative attitudes toward same-sex and opposite-sex sexual relationships because conservative attitudes benefit their mating strategies (e.g., monogamy). Certain mating market cues, however, can shift attitudes. In two experiments recruiting Americans and Australians (total N = 1298), we took a data-driven approach to test whether experimental manipulations of (1) promiscuity among either homosexuals (gays and lesbians) or heterosexuals and (2) the financial amount that either homosexuals (gays and lesbians) or heterosexuals invest in weddings would shift attitudes toward same-sex marriage, dating, and romantic spending. In Experiment 1, we did not replicate previous findings that homosexual promiscuity affects attitudes to same-sex marriage, nor did we find any effects of priming heterosexual promiscuity. However, priming participants with the notion that either homosexuals or heterosexuals were highly promiscuous increased support for traditional relationship norms among sexually restricted Australian (but not American) men. This effect was smaller when we controlled for participant sexual orientation, because primes of high homosexual or heterosexual promiscuity increased support for these traditional norms in exclusively heterosexual Australians, but decreased support in non-heterosexual Australians. Experiment 2 found that American and Australian men's opposition to same-sex marriage increased when they were led to believe that either homosexual or heterosexual weddings were cheap, even when controlling for participant sexual orientation. Overall, results provide some support for the argument that mating market cues affect attitudes toward sexual relationships.

Status anxiety mediates the positive relationship between income inequality and sexualization.

Income inequality generates and amplifies incentives, particularly incentives for individuals to elevate or maintain their status, with important consequences for the individuals involved and aggregate outcomes for their societies [R. G. Wilkinson, K. E. Pickett, Annu. Rev. Sociol. 35, 493-511 (2009)]. Economically unequal environments intensify men's competition for status, respect, and, ultimately, mating opportunities, thus elevating aggregate rates of violent crime and homicide [M. Daly, M. Wilson, Evolutionary Psychology and Motivation (2001)]. Recent evidence shows that women are more likely to post "sexy selfies" on social media and that they spend more on beautification in places where inequality is high rather than low [K. R. Blake, B. Bastian, T. F. Denson, et al., Proc. Natl. Acad. Sci. U.S.A. 115, 8722-8727 (2018)]. Here we test experimentally for causal links between income inequality and individual self-sexualization and status-related competition. We show that manipulating income inequality in a role-playing task indirectly increases women's intentions to wear revealing clothing and that it does so by increasing women's anxiety about their place in the social hierarchy. The effects are not better accounted for by wealth/poverty than by inequality or by modeling anxiety about same-sex competitors in place of status anxiety. The results indicate that women's appearance enhancement is partly driven by status-related goals.

Sex-dependent selection, ageing, and implications for "staying alive".

Incorporating theoretic insights from ageing biology could advance the "staying alive" hypothesis. Higher male extrinsic mortality can weaken selection against ageing-related diseases and self-preservation, leading to high male intrinsic mortality. This may incidentally result in female-biased longevity-promoting traits, a possibility that will require rigorous testing in order to disentangle from the adaptive self-preservation hypothesis presented in the target article.

Income inequality not gender inequality positively covaries with female sexualization on social media.

Publicly displayed, sexualized depictions of women have proliferated, enabled by new communication technologies, including the internet and mobile devices. These depictions are often claimed to be outcomes of a culture of gender inequality and female oppression, but, paradoxically, recent rises in sexualization are most notable in societies that have made strong progress toward gender parity. Few empirical tests of the relation between gender inequality and sexualization exist, and there are even fewer tests of alternative hypotheses. We examined aggregate patterns in 68,562 sexualized self-portrait photographs ("sexy selfies") shared publicly on Twitter and Instagram and their association with city-, county-, and cross-national indicators of gender inequality. We then investigated the association between sexy-selfie prevalence and income inequality, positing that sexualization-a marker of high female competition-is greater in environments in which incomes are unequal and people are preoccupied with relative social standing. Among 5,567 US cities and 1,622 US counties, areas with relatively more sexy selfies were more economically unequal but not more gender oppressive. A complementary pattern emerged cross-nationally (113 nations): Income inequality positively covaried with sexy-selfie prevalence, particularly within more developed nations. To externally validate our findings, we investigated and confirmed that economically unequal (but not gender-oppressive) areas in the United States also had greater aggregate sales in goods and services related to female physical appearance enhancement (beauty salons and women's clothing). Here, we provide an empirical understanding of what female sexualization reflects in societies and why it proliferates.

Condition-Dependent Mutual Mate Preference and Intersexual Genetic Correlations for Mating Activity.

Although mating represents a mutual interaction, the study of mate preferences has long focused on choice in one sex and preferred traits in the other. This has certainly been the case in the study of the costs and condition-dependent expression of mating preferences, with the majority of studies concerning female preference. The condition dependence and genetic architecture of mutual mate preferences remain largely unstudied, despite their likely relevance for the evolution of preferences and of mating behavior more generally. Here we measured (a) male and female mate preferences and (b) intersexual genetic correlations for the mating activity in pedigreed populations of southern field crickets (Gryllus bimaculatus) raised on a favorable (free-choice) or a stressful (protein-deprived) diet. In the favorable dietary environment, mutual mate preferences were strong, and the intersexual genetic covariance for mating activity was not different from one. However, in the stressful dietary environment, mutual mate preferences were weak, and the intersexual genetic covariance for mating activity was significantly smaller than one. Altogether, our results show that diet environments affect the expression of genetic variation in mating behaviors: when the environment is stressful, both (a) the strength of mutual mate preference and (b) intersexual genetic covariance for mating activity tend to be weaker. This implies that mating dynamics strongly vary across environments.

Man, Woman, "Other": Factors Associated with Nonbinary Gender Identification.

Using a unique dataset of 7479 respondents to the online Australian Sex Survey (July-September 2016), we explored factors relevant for individuals who self-identify as one of the many possible nonbinary gender options (i.e., not man or woman). Our results identified significant sex differences in such factors; in particular, a positive association between female height, higher educational levels, and greater same-sex attraction (female-female) versus a negative effect of lower income levels and more offspring. With respect to sex similarities, older males and females, heterosexuals, those with lower educational levels, and those living outside capital cities were all more likely to identify as the historically dichotomous gender options. These factors associated with nonbinary gender identification were also more multifaceted for females than for males, although our interaction terms demonstrated that younger females (relative to younger males) and nonheterosexuals (relative to heterosexuals) were more likely to identify as nonbinary. These effects were reversed, however, in the older cohort. Because gender can have such significant lifetime impacts for both the individual and society as a whole, our findings strongly suggest the need for further research into factors that impact gender diversity.

Superoxide dismutase deficiency impairs olfactory sexual signaling and alters bioenergetic function in mice.

Oxidative stress (an overproduction of reactive oxygen species in relation to defense mechanisms) may restrict investment in life history traits, such as growth, reproduction, lifespan, and the production of sexual signals to attract mates. The constraint on sexual signaling by oxidative stress is of particular interest because it has been proposed as a mechanism ensuring that only good-quality males produce the most attractive sexual signals. Despite these predictions, evidence supporting this theory is, at best, equivocal. We used a superoxide dismutase knockout mouse to demonstrate that oxidative stress directly impairs investment in morphological (preputial glands) and molecular (major urinary proteins) components of olfactory signaling essential for mate attraction. By maintaining males in a much more competitive environment than usual for mouse laboratory experiments, we also revealed a range of phenotypes of superoxide dismutase deficiency not observed in previous studies of this mouse model. This range included impaired bioenergetic function, which was undetectable in the control environment of this study. We urge further examination of model organisms in seminatural conditions and more competitive laboratory environments, as important phenotypes can be exposed under these more demanding conditions.

Diversification of the eutherian placenta is associated with changes in the pace of life.

Few mammalian organs vary as dramatically among species as the placenta. This variation is remarkable considering that the placenta's primary function--transfer of nutrients and waste between mother and offspring--does not differ among species. Evolutionary changes in placental morphology remain poorly understood, with suggestions that parent-offspring conflict or evolutionary changes in life history might drive placental evolution. Here we demonstrate that life history differences among eutherian mammals are associated with major transitions in maternofetal interdigitation and placental invasiveness. We show that the repeated evolution of villous interdigitation is associated with reduced offspring production early in life and an increased lifespan. Further changes in placental morphology that reestablish a larger surface area are also associated with a change back to greater offspring production. After controlling for these differences in interdigitation, we also show that the least invasive placental type is associated with a fast pace of life. We predict that selection for a faster pace of life intensifies parent-offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the fetus and alter their relative allocation to offspring production across life.

A genetic reduction in antioxidant function causes elevated aggression in mice.

Male-male aggression can have a large influence on access to mates, particularly in highly territorial animals such as mice. It has been suggested that males with impaired antioxidant defence and a consequential increased susceptibility to oxidative stress may have a reduced ability to invest in aggressive behaviours, which could limit their mating opportunities and reproductive success. Oxidative stress occurs as a result of an uncontrolled over-production of reactive oxygen species (ROS) in relation to defence mechanisms (such as antioxidants), and can cause damage to a variety of different cellular components. Impairments in specific aspects of antioxidant defence, leading to oxidative stress, can limit investment in some reproductive traits in males, such as sperm quality and the production of sexual signals to attract mates. However, a direct effect of impaired antioxidant defence on aggressive behaviour has not, to our knowledge, been reported. In this study, we demonstrate that mice with experimentally elevated sensitivity to oxidative stress (through inhibition of copper-zinc superoxide dismutase, Sod1) actually show the opposite response to previous predictions. Males completely deficient in SOD1 are more aggressive than both wild-type males and males that express 50% of this antioxidant enzyme. They are also faster to attack another male. The cause of this increased aggression is unknown, but this result highlights that aggressive behaviour in mice is not highly constrained by inhibited Sod1 expression, in contrast to other reproductive traits known to be impaired in this mouse model.

Experimental evidence that litter size imposes an oxidative challenge to offspring.

The post-natal environment in which young develop can substantially impact development, adult phenotype and fitness. In wild mice, competition among litter-mates affects development rate and adult behaviour. We manipulated post-natal litter size in a cross-fostering design to investigate the effects of enlarged and reduced litter sizes on sexual signalling, oxidative stress and the links between them. Oxidative stress causes somatic damage that can limit reproductive success and lifespan, and is predicted to mediate investment in life-history traits, including sexual signals. We predicted that litter enlargement would cause an increase in potential oxidative stress, inhibit growth and reduce sexual signalling in male mice. Males reared in enlarged litters were smaller at weaning and, despite rapid growth immediately after weaning, remained smaller at 10 weeks of age than those reared in smaller litters. Females from enlarged litters were consistently smaller throughout post-weaning development and showed no increase in growth rate compared with females from reduced litters. In enlarged litters, protein thiol concentration was lower at weaning in the liver and kidneys, with this trend continuing at 10 weeks of age in the kidneys only. Aconitase enzyme activity was also lower in mice from enlarged litters at weaning and 10 weeks of age in the kidneys. Male mice from enlarged litters scent marked more frequently and had larger preputial glands than those from reduced litters, indicating greater sexual signalling investment irrespective of this increased oxidative challenge. The results of this study are the first to reveal oxidative costs of developmental stress in small mammals.

Long-term effect of social interactions on behavioral plasticity and lifetime mating success.

Behavioral traits often change over an individual's lifetime. Experience, physiological senescence, and age-dependent differences in optimal behavior can, in theory, all cause longitudinal behavioral changes. Yet most studies of behavioral plasticity and selection on behavior focus on short-term population-level responses to social factors such as conspecific density or sex ratio. Longer-term effects of social interactions on individual behavior have rarely been tested. Here we tested these effects by exposing male water striders (Hemiptera: Gerridae) to two different social conditions throughout their lifetime; we call these the nonsocial and social treatments. We then measured each male's lifetime mating success and individual behavioral plasticity by observing four different behaviors (exploring a novel environment, dispersal ability, sex-recognition sensitivity, and tendency to remount a resistant female after being dislodged) every 2 weeks. The social environment influenced individual variation in behavioral plasticity as well as population-level behavioral plasticity. Moreover, when we calculated linear selection gradients of individual behavioral traits and their plasticities on lifetime mating success, male remounting tendency and individual plasticity in exploration ability were likely to be the most important factors explaining variation in male lifetime mating success. In conclusion, the variation in social interactions throughout an individual's lifetime contributes to the individual variation in behavioral plasticity, which can significantly affect a male's lifetime fitness.

Negative frequency-dependent preferences and variation in male facial hair.

Negative frequency-dependent sexual selection maintains striking polymorphisms in secondary sexual traits in several animal species. Here, we test whether frequency of beardedness modulates perceived attractiveness of men's facial hair, a secondary sexual trait subject to considerable cultural variation. We first showed participants a suite of faces, within which we manipulated the frequency of beard thicknesses and then measured preferences for four standard levels of beardedness. Women and men judged heavy stubble and full beards more attractive when presented in treatments where beards were rare than when they were common, with intermediate preferences when intermediate frequencies of beardedness were presented. Likewise, clean-shaven faces were least attractive when clean-shaven faces were most common and more attractive when rare. This pattern in preferences is consistent with negative frequency-dependent selection.

Sexual selection and speciation in the Anthropocene.

Anthropogenic change threatens global biodiversity by causing severe ecological disturbance and extinction. Here, we consider the effects of anthropogenic change on one process that generates biodiversity. Sexual selection (a potent evolutionary force and driver of speciation) is highly sensitive to the environment and, thus, vulnerable to anthropogenic ecological change. Anthropogenic alterations to sexual display and mate preference can make it harder to distinguish between conspecific and heterospecific mates or can weaken divergence via sexual selection, leading to higher rates of hybridization and biodiversity loss. Occasionally, anthropogenically altered sexual selection can abet diversification, but this appears less likely than biodiversity loss. In our rapidly changing world, a full understanding of sexual selection and speciation requires a global change perspective.

Copper-zinc superoxide dismutase deficiency impairs sperm motility and in vivo fertility.

Oxidative stress, overproduction of reactive oxygen species (ROS) in relation to defence mechanisms, is considered to be a major cause of male infertility. For protection against the deleterious effects of ROS, animals have a variety of enzymatic antioxidants that reduce these molecules to less reactive forms. The physiological role of these antioxidants in vivo has been explored extensively through genetic inhibition of gene expression; surprisingly, many of these animals remain fertile in spite of increased oxidative stress. Copper-zinc superoxide dismutase-deficient (Sod1(-/-)) male mice are one such example for which in vivo fertility has been repeatedly reported as normal, although examination of fertility has consisted of simply pairing animals of the same strain and checking for litters. This is a fairly low criterion by which to assess fertility. Herein, we show that Sod1-deficient males have zero fertilisation success in sperm competition trials that pit them against wild-type males of an otherwise identical genetic background and are almost completely infertile when mated singly with females of a different genotype. We also show that various aspects of sperm motility and function are impaired in Sod1-deficient mice. Testing the breeding capabilities of mice under more ecologically relevant conditions and with females of different genotypes may help reveal additional physiological causes of infertility.

Physiological adaptations to reproduction. II. Mitochondrial adjustments in livers of lactating mice.

Reproduction imposes significant costs and is characterized by an increased energy demand. As a consequence, individuals adjust their cellular structure and function in response to this physiological constraint. Because mitochondria are central to energy production, changes in their functional properties are likely to occur during reproduction. Such changes could cause adjustments in reactive oxygen species (ROS) production and consequently in oxidative stress levels. In this study, we investigated several mechanisms involved in energy production, including mitochondrial respiration at different steps of the electron transport system (ETS) and related the results to citrate synthase activity in the liver of non-reproductive and reproductive (two and eight pups) female house mice at peak lactation. Whereas we did not find differences between females having different litter sizes, liver mitochondria of reproductive females showed lower ETS activity and an increase in mitochondrial density when compared with the non-reproductive females. Although it is possible that these changes were due to combined processes involved in reproduction and not to the relative investment in lactation, we propose that the mitochondrial adjustment in liver might help to spare substrates and therefore energy for milk production in the mammary gland. Moreover, our results suggest that these changes lead to an increase in ROS production that subsequently upregulates antioxidant defence activity and decreases oxidative stress.

Physiological adaptations to reproduction. I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice.

Life history theory suggests that investment in reproduction can trade off against growth, longevity and both reproduction and performance later in life. One possible reason for this trade-off is that reproduction directly causes somatic damage. Oxidative stress, an overproduction of reactive oxygen species in relation to cellular defences, can correlate with reproductive investment and has been implicated as a pathway leading to senescence. This has led to the suggestion that this aspect of physiology could be an important mechanism underlying the trade-off between reproduction and lifespan. We manipulated female reproductive investment to test whether oxidative stress increases with reproduction in mice. Each female's pups were cross-fostered to produce litters of either two or eight, representing low and high levels of reproductive investment for wild mice. No differences were observed between reproductive groups at peak lactation for several markers of oxidative stress in the heart and gastrocnemius muscle. Surprisingly, oxidative damage to proteins was lower in the livers of females with a litter size of eight than in females with two pups or non-reproductive control females. While protein oxidation decreased, activity levels of the antioxidant enzyme superoxide dismutase increased in the liver, suggesting this may be one pathway used to protect against oxidative stress. Our results highlight the need for caution when interpreting correlative relationships and suggest that oxidative stress does not increase with enhanced reproductive effort during lactation.

Societies should not ignore their incel problem.

Involuntarily celibate men ('incels') commonly advocate for societal disruption, including violence toward women. Their anger can make them susceptible to radicalization, revolution, or reactionary hostility. Research efforts aimed at identifying the causes and consequences of incels' beliefs are needed to address this growing problem.