Sexual selection and the evolution of behavior, morphology, neuroanatomy and genes in humans and other primates.

Neuroscience and Biobehavioral Reviews 46 (2014) 579–590

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Sexual selection and the evolution of behavior, morphology, neuroanatomy and genes in humans and other primates Roscoe Stanyon ∗ , Francesca Bigoni Department of Biology, University of Florence, Anthropology laboratories, via del Proconsolo 12, 50122 Florence, Italy

a r t i c l e

i n f o

Article history: Received 27 January 2014 Received in revised form 20 September 2014 Accepted 1 October 2014 Available online 14 October 2014 Keywords: Sexual dimorphism Social complexity Female competition Non-conceptive mating Brain size Epigenetics Gene expression

a b s t r a c t Explaining human evolution means developing hypotheses about the occurrence of sex differences in the brain. Neuroanatomy is significantly influenced by sexual selection, involving the cognitive domain through competition for mates and mate choice. Male neuroanatomy emphasizes subcortical brain areas and visual-spatial skills whereas that of females emphasizes the neocortex and social cognitive areas. In primate species with high degrees of male competition, areas of the brain dealing with aggression are emphasized. Females have higher mirror neuron activity scores than males. Hundreds of genes differ in expression profiles between males and females. Sexually selected differences in gene expression can produce neuroanatomical sex differences. A feedback system links genes, gene expression, hormones, morphology, social structure and behavior. Sex differences, often through female choice, can be rapidly modulated by socialization. Human evolution is a dramatic case of how a trend toward pair bonding and monogamy lowered male competition and increased female choice as a necessary step in releasing the cognitive potential of our species. © 2014 Elsevier Ltd. All rights reserved.

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Social structure and mating systems affect body sex-dimorphism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Female promiscuity and cryptic mate choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Sperm competition and genitalia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Increasing focus on female–female competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Female secondary sexual characteristic: armaments or ornaments? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The impact of sexual selection on primate brains and neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Gross neuroanatomical differences between sexes: from male competition to female empathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Sexually selected sex differences in gene expression can produce neuroanatomical differences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Epigenetics, genomic imprinting and hormones can cause sexual dimorphism in neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Social environment influences differences in neuroanatomy between males and females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A scenario of human evolution linking sexual selection, behavior, social structure, gene expression and neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . 5.1. Uniqueness of human reproductive anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Sexual selection drove a clear trend toward pair bonding and increased paternal investment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Decrease of sexual dimorphism in the genus Homo is evidence of increased female choice and decreased male competition . . . . . . . . . . 5.4. The neuroanatomy of pair-bonding and stable social system in the human lineage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. Tel.: +39 055 2757738. E-mail address: roscoe.stanyon@unifi.it (R. Stanyon). http://dx.doi.org/10.1016/j.neubiorev.2014.10.001 0149-7634/© 2014 Elsevier Ltd. All rights reserved.

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R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590

1. Introduction The outlandish size of the human brain has always fascinated evolutionary biologists. Explaining human evolution has in large part meant developing hypotheses about why humans have brains three times the size of their nearest primate relatives (Sherwood et al., 2008) and to what extent the brain may differ in a sex specific manner (Becker et al., 2008). Darwin (1871) developed the theory of sexual selection to explain sexual dimorphism, the differences between males and females of the same species. He proposed that behavioral differences between males and females were at the root of sexual selection. Males competed for access to females whereas the most notable female characteristic was to choose the best mate among male competitors. Darwin proposed that the large brain of humans was driven by sexual selection to its absurd and sex-dependent proportion. As with the peacock’s resplendent tail, males were the sex most influenced by sexual selection, so that “the average standard of mental power in man must be above that of women. . .thus man has ultimately become superior to woman”. However, whereas Darwin’s simplified and ridiculous view of women is typical of the Victorian age (Birkhead, 2010), his idea that sexual selection could have a profound influence on the brain is now a lively field of inquiry also in humans (Cahill, 2006; Miller, 2011). How sexual selection – which implies behavioral flexibility, cognitive abilities and different roles between sexes – has modulated primate morphology as well as complex neuroanatomy and gene expression is just beginning to be appreciated (Dunbar, 2007, 2009; Lindenfors et al., 2007; Montgomery and Mundy, 2013). Studies now show that sexual dimorphism in neuroanatomy of primates is significantly influenced by sex-biased behavioral traits that enhance fitness in different mating systems and social structures. Sex differences in neuroanatomy are part of a feedback system linking social and mating structures, behavior, and gene expression to sexual selection. New light is being shed on the evolution of humans by our improved understanding of the processes and mechanisms of sexual selection during primate evolution (Cachel, 2006, 2009; Sherwood et al., 2008; Chapais, 2013; Fleagle, 2013).

2. Social structure and mating systems affect body sex-dimorphism It is widely acknowledged that sexual selection is modulated by variations in social structure and the reverse, but it was not an easy task to dissect out the many contributing components. Primate social organization is highly dependent on ecological variables that influence the spatiotemporal distribution of females. It is no banal conclusion that males follow females (Altmann, 1990). Female distribution then is a major driving factor in determining variation in social and mating systems (Carnes et al., 2011; Lindenfors et al., 2004). Primates have a wide range of mating systems including unusual multimale–multifemale groups (Ostner et al., 2013). The mating systems of living primates with simplification are classified as monogamous (pairs), polygynous (one male with multiple females), polyandrous (one female with multiple males) and polygynandrous (multimale–multifemale) (Martin, 2007). Mating systems are apparently not strongly influenced by primate phylogeny (Fig. 1), but on the other hand sexual dimorphism is strongly correlated with the mating system (Fig. 2). The peak of sex-dimorphism occurs in case of the harem (one male–multifemale, i.e. gorilla) or when a male is associated with a female just for mating, as in orangutan (Fleagle, 2013). Social and mating systems determine an incredible range of both morphological and behavioral traits. Darwin (1871) discussed sex differences in size, canine teeth as well as color, length of pelage and

sexual skin in various polygamous species of primates in relation to both male fights for access to a mate and female “taste for the beautiful”; nevertheless, Darwin only vaguely connected these traits to the mating types recognized today. The degree of male competition depends on both the number of females in groups and female reproductive synchrony (Nunn, 1999). Polygynous species are the most sexually dimorphic in body and canine size while monogamous species have almost no sexual dimorphism for these armaments as well as for aesthetic traits. Male ornaments are rare among mammals in comparison to birds where male ornaments were considered as products of male–male competition. Nevertheless, male skin coloration was interpreted as an attractive sexual signal in rhesus macaques (Waitt et al., 2003; Dubuc et al., 2014) and in mandrills (Setchell and Jean Wickings, 2005). Such coloration is status-dependent, suggesting a dual utility of armaments/ornaments in sexual selection (Berglund et al., 1996). 2.1. Female promiscuity and cryptic mate choice Females instead of males are now the focus of many sexual selection studies, due to the key role of female mate choice. Rather than being a cooperative venture between the sexes, sexual reproduction is now viewed in terms of conflicts of interests among rivals of the same sex but also between males and females (Birkhead, 2010). Females may increase reproductive success through promiscuity, especially in multimale–multifemale groups. Darwin did not account for female promiscuity; he apparently thought that female choice was keyed to select one male, not to mate with multiple males. It was only in the last 50 years that the implication of female promiscuity became clear (Birkhead, 2010). Through promiscuity females can confound paternity, avoid infanticide and acquire genetically compatible sperm. Females also increase their mate choice toward high quality males for critical copulation and post-copulatory mate choice. “Cryptic female choice” (sensu Eberhard 1996) can operate to maximize female choice by disguising or concealing ovulation to relax male coercion (Muller et al., 2007; Stumpf and Boesch, 2010). Even the pH of the primate vagina can determine a drastic selection of sperm (Dixson and Anderson, 2004) and primate seminal fluids must adapt to neutralize low pH. In primates these female strategies are facilitated by lengthy periods of sexual activity around ovulation. 2.2. Sperm competition and genitalia For males the quantity and quality (vigor and speed) of sperm ejaculated into the female reproductive tract can be a crucial counter strategy to female promiscuity (Anderson et al., 2007). Sperm competition helps explain the variability found in primate genitals. There is an association between relative testis size and primate mating systems (Dixson and Mundy, 1994a,b; Harcourt and Gardiner, 1994; Harcourt et al., 1981; Hosken and Stockley, 2004; Shamloul et al., 2010; Verrell, 1992). Sperm competition is low in one male mating systems and here the testes are generally smaller. Sperm competition should be highest in multimale–multifemale systems due to promiscuous mating and indeed testes size is much larger. Relative testes size is now taken as a good indicator of the strength of sperm competition. Sperm vigor follows the same correlation. Faster sperm are found in groups of multiple adults of both sexes while the slowest sperm are found in one male mating systems (Nascimento et al., 2008). The morphology of the penis (head, length and width) may evolve to both safely deposit sperm and to facilitate the removal of competitors’ sperm. It has been hypothesized that one function of larger penises would be both to remove rivals’ sperm


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Fig. 1. A phylogenetic scheme of Simiiformes at the genus level. The various colors correspond to the predominant social mating system: red = multimale–multifemale (polygynandrous), green = single male–multifemale, blue = monogamous pairs, pink = polyandrous, yellow = fusion–fission, orange = solitary males. Modified from Springer et al. (2012) (http://creativecommons.org/licenses/by/2.5/); data on social structure are from Fleagle (2013). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

and deposit sperm out of reach; therefore they should be larger in multimale–multifemale societies. However, the relationship of social structure with penis size is not clear-cut. Both competition and female choice should influence penile morphologies. It does appear that a longer penis is associated with multimale–multifemale species and dispersed mating systems where sperm competition should be high (Dixson, 2002). Part of this relationship is certainly due to the fact that sexual swelling, i.e. the tumescence of perineal skin in some female primates during the periovulatory period (see Fig. 3, makes the entrance to the vagina longer.

3. Increasing focus on female–female competition Beyond female distribution and female mate choice, there can be no doubt that female-female competition for dominance rank influences reproductive success (Cant and Young, 2013). Darwin did not consider female competition as a part of sexual selection and it has historically received much less attention than male sexual competition (Rubenstein, 2012). The importance of competition between females has garnered increased attention (Clutton-Brock, 2007; Clutton-Brock and Huchard, 2013; Hrdy, 2013; Stockley and

Campbell, 2013). Traditionally, it was thought that competition between females was mostly over food. Differences in female relationships and female group size can be dependent on ecological variables that may be conducted back to food resources (Lindenfors and Tullberg, 2011). It is uncertain how much of this competition falls under the umbrella of sexual selection. Recently there has been some attempt to propose that sexual selection is just a subset of social selection (Rubenstein, 2012). Whatever the relationship between social selection and sexual selection, we can safely conclude that mating competition intensity –among males as well as females – and other parameters of sexual selection – can influence the group size and the genetic relatedness between group members. Female–female competition may consist in a fine social manipulation. Pregnant gorilla females are known to copulate only when other females are receptive. The hypothesis is that these matings are a strategy by which pregnant females attempt to minimize male interest in other females, while reinforcing their own status and potentially delaying conception in others (Doran-Sheehy et al., 2009). Thus female mating competition may be a factor in the evolution of non-conceptive mating (Furuichi et al., 2014). A similar interpretation can be given to the finding that female bear macaques synchronize copulations, instead of cycles (Furtbauer

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3.1. Female secondary sexual characteristic: armaments or ornaments?

Fig. 2. Sexual dimorphism in body size in Simiiformes primates in relationship to social structure (see color code in Fig. 1): mmmf = multimale–multifemale (red), smmf = single male–mutlifemale (green), sol m = solitary males (orange) consort with females only for mating, fufi = fusion–fission (yellow), mo = monogamy (blue), pa = polyandry (pink), HSA = Homo sapiens (black). Platyrrhine (New World) Primates = P and Catarrhine (Old World) Primates = C. Graph (a) shows the average adult male weight divided by average adult female weight. Graph (b) shows the percent difference of males to females. Data are from Fleagle (2013). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

et al., 2011). Copulatory calls in chimpanzees are used for social manipulation of both males and other females (Townsend et al., 2008). Yet female competition is not limited to these subtle maneuvers and may escalate into outright physical aggression. In the golden monkey more than 75% of the harassers were adult or sub-adult females (Qi et al., 2011). Sexual interference by females and infanticide can be considered more direct expressions of female competition. The importance of female infanticide is probably underestimated. In chimpanzees, intragroup infanticide is often perpetrated by females (Pusey and Schroepfer-Walker, 2013; Stockley and Bro-Jørgensen, 2011; Townsend et al., 2007; Williams et al., 2008). Overall, the ultimate effects of female competition are harder to measure. Primate females are undoubtedly capable of competing and fighting over limiting resources when necessary. In some species females may compete over males. There is apparently some correlation between increasing group size and decreasing female reproductive success. In yellow baboons the direct aggression of dominant females and matrilineage kin toward other females effectively lower the victims’ reproductive success (Stockley and Bro-Jørgensen, 2011; Stockley and Campbell, 2013; Young and Bennett, 2013). In chimpanzees, as in many primates species, highranking infant survival, faster maturing daughters, and more rapid production of young are phenomena linked to female competition (Pusey et al., 1997).

Female facial coloration has been traditionally viewed as a sexual signal (Dixson, 1983; Fink et al., 2006). For example in mandrills it is more vivid in dominant females and during fertile periods (Setchell et al., 2006). It is now better appreciated that primate females may have secondary sexual characters that are as striking as those of males (i.e. swellings Fig. 3), but it is difficult to separate the effects of female choice from female competition (Rubenstein, 2012). The selective forces behind swellings and other female secondary sexual characteristics are likely to be multifactorial. One hypothesis is that exaggerated sexual swellings are ornaments indicative of female competition for males and are not just limited to promoting paternity confusion among males. Swellings may be honest indicators of quality (Zahavi, 1975) and females can use them to obtain male attention and bonding although this may often be difficult to establish empirically (Zinner et al., 2002). In several species differences in the relative size of the swelling are positively correlated with the female’s body condition and reproductive success (Huchard et al., 2009). If they are honest indicators then males can increase fitness by mating with these females and maintaining relationships with them. In this manner females can tap into male aid, support and paternal care for a more prolonged period of time than simple copulation. Therefore female competition in this case could be over male contribution to parental care. Recent work in baboons, where exaggerated swelling are present, shows that lactating females maintain close associations with adult males during the most vulnerable period of an infant’s life (Ostner et al., 2013). The hypothesis is that a male’s mating success is enhanced if he bonds with a specific female. This strategy is expected to be more common in subordinate males who select to invest in a particular female as opposed to the riskier business of sneaking copulations with multiple females (Ostner et al., 2013). Importantly, stability in female–male partners may develop in multimale–multifemale groups. In rhesus macaques, males are known to have better paternity success with females that they have bonded to (Kulik et al., 2012). Overall, however, female competition must differ from male competition due to the greater investment usually made by females in producing and rearing offspring (Stockley and Campbell, 2013) and conflicts among females are most often resolved without overt physical contests (Young and Bennett, 2013). An example of behavior regulating social tension could be the sexual rubbing between female bonobos (De Waal, 2006; Clay and de Waal, 2014; Ryu et al., 2014, Fig. 3). Current neuropsychological evidence shows that females have been selected to avoid direct conflict. Human females have heightened amygdala reactivity to threatening stimuli, giving them superior prefrontal cortical control over emotional behavior (Campbell, 2013). We know that girls use strategies that minimize direct conflict and disguise competition (Benenson, 2013). Reproductive conflict among human females is most frequently resolved through social castigation, exclusion and punishment (Cant and Young, 2013).

4. The impact of sexual selection on primate brains and neuroanatomy The fact that primates living in larger groups have larger brains is a simple but elegant demonstration that neuroanatomy is related to and driven by sociality (Dunbar and Shultz, 2007). However, the underlying relationship is with social complexity (“the social brain hypothesis”, Dunbar, 2009) and with mating systems in primates. We have already seen that there are strong morphological correlates between mating systems, body and canine dimorphism,


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Fig. 3. Two bonobo (Pan paniscus) females engaged in genital rubbing. It is thought that genital rubbing enforces bonds between females. The exaggerated, genital swelling of both females is evident. Human females never show swellings in the anal/genital region while bonobo adult females are never without swellings even if they may follow a temporal phase. Both promote the same result: concealed ovulation. Swellings in human probably due to the evolution of bipedalism have moved to the front as permanently swollen breast. Genital rubbing between adult bonobo females also consolidates vital female relationships, but recent research shows that the female in top position is usually superior in rank (unpublished data). Photograph courtesy of Elisabetta Palagi.

ornaments, as well as sperm competition and testes size. Additionally, there is a significant negative evolutionary relationship between relative brain size and the level of male competition for mates. In short, larger brains are associated with lowered male competition and monogamous mating systems in both primates (Fig. 4; Schillaci, 2006) and birds (West, 2014). In line with Dunbar’s social brain hypothesis we would conclude that monogamy and pair bonding is cognitively more demanding. Deception and detecting cheating would have pushed brain size in a sort of arms race. Sexual dimorphism in brain size can also be explored by genomic analysis. Human microcephaly is a heterogeneous group of neurodevelopmental disorders that cause infants to have smaller heads than normal. Congenital microcephaly is frequently inherited. Over the last decade genomic methods have identified genetic loci responsible for microcephaly. Genes that cause congenital microcephaly control important aspects of neural development. These genes are apparently involved in the evolutionary explosion of cortical size that characterizes primates and especially humans. Due to their acceleration in the human line, genes linked to human primary microcephaly have also received much attention from evolutionary biologists and anthropologists. Two examples are microcephalin (MCPH1) and abnormal spindle-like microcephaly (ASPM). In clinical cases brain size is reduced in volume to a size comparable with that of early hominids. Studies showed that both genes have undergone positive selection during great ape evolution (Ponting and Jackson, 2005). Montgomery et al. (2011) studied these genes in 21 primate species and surprisingly found that humans were not the only species, which had experienced accelerated evolution in the genes they considered. Later Montgomery and Mundy (2013) reported on the role of four microcephaly genes in the evolution of sexual dimorphism in primate brain size. One aim of the study was to understand the phenotypic relevance of selection acting on these genes. Sexdependent associations were found between variation in three

microcephaly genes and human brain size. They concluded that these genes have contributed to the evolution of sexual dimorphism in the brain and neuroanatomy of primates. Reinius et al. (2008) reported on a conserved sexual genomic signature in primate brains. They identified genes with sex differences in brain expression levels in the cortex regions of a New World monkey, an Old World primate and humans. They discovered literally hundreds of genes with different expression profiles between males and females. Many of these genes had higher expression profiles in females. Many of these profiles were conserved between species. However, they could only speculate that these gene profiles may underlie important functional differences between the sexes, with possible importance during primate evolution. Later Pointer et al. (2013) concluded that exaggerated male sexual dimorphism in turkeys was associated with the masculinization of gene expression. According to these authors, sex-biased gene expression is at the root of the majority of sexually dimorphic phenotypes in these birds. It seems likely that gene expression is also at work in primates in a similar fashion. 4.1. Gross neuroanatomical differences between sexes: from male competition to female empathy Evidence now shows that certainly there is a detectable sexual selection effect on primate neuroanatomy (Dunbar, 2007). Gross anatomical differences exist between male and female primate neuroanatomy that must be related to sexual selection. Male sociality is more related to subcortical brain areas whereas that of females is more related to the neocortex (Lindenfors et al., 2007). These findings would convincingly argue for a mosaic view of neuroanatomy both between and within species (male vs. female). A recent study confirmed these results by comparing prefrontal volumes of white/grey matter ratios in males and females of 10 primate species. Human females evolve less and males more white/grey

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Fig. 4. Error-bar plots of residuals from the least-squares regressions of brain (a and b) and testis (c and d) weights on body weight, and sexual mass dimorphism values (e and f) by mating system and female promiscuity determinations. Variables were loge—transformed prior to regression analysis. Error bars represent one standard error of the mean. Mating system: MMMF, multi-male/multi-female; PA, polyandrous; Mon, monogamous; SM single male. An increase in body size dimorphism (E-F) is associated with a decrease in relative brain size (A-B), whereas sperm competition does not effect relative brain size (C-D). From Schillaci (2006). doi:10.1371/journal.pone.0000062 http://creativecommons.org/licenses/by/2.5/).

matter volume than predicted for a non-human anthropoid female (Smaers et al., 2012). Females had more grey matter vs. white matter than male especially in the left hemisphere (Fig. 5). The left hemisphere is involved in affiliation, social bonding and empathy. These results show that sexual dimorphism and laterality are significant factors in the evolution of the human brain. Almost all neuroanatomical data support the conclusion that the degree of male competition is positively correlated with neuroanatomy that controls autonomic functions and sensory-motor skills as well as those relating to aggression including mesencephalon, diencephalon and amygdala size and a reduction of the septum (Lindenfors et al., 2007). The hypothesis is that in species with high degrees of male competition, areas of the brain dealing with aggression are emphasized (Lindenfors and Tullberg, 2011). Recently MR brain imaging was used to compare male and female human brains. Overall 121 subjects including 67 females were studied. The results confirmed morphometric findings and discriminated differences in gray-matter and microstructures in cortical and subcortical areas. Sex differences were found among others to favor females in social cognitive areas and males in visual-spatial skills (Feis et al., 2013). Mirror neurons are another area of the neuroanatomy where we find differences between males and females. A mirror neuron

fires both when an animal acts and when the animal observes the identical action performed by another. Thus the neuron appears to mirror the actions of the other just as if it was performing the act. Mirror neurons were discovered in macaques and at first were thought to be restricted to Old World primates (Ferrari et al., 2009; Cook et al., 2014). We now know that mirror neurons are found outside primates and even in birds (Keysers and Gazzola, 2009), although they have been most extensively studied in primates. Mirror neurons are believed to be important in social animals as they provide a neurological basis for connecting individuals and for understanding the actions of others, through a perceptionaction mechanism. Mirror neurons are thought to be important in imitation, learning, empathy and self-awareness. Long standing circumstantial evidence suggests that there were sex differences in traits linked to mirror neurons, most notable empathy. Females generally score higher in tests of empathy, sensitivity and emotional recognition. Therefore the hypothesis is that females should be more richly endowed with mirror neurons. Sex differences in mirror neurons were documented in humans (Cheng et al., 2008) using neurophysiological methods. Females had higher values than males. These few data support the view that the sex differences in mirror neurons were generated by sexual selection in the brain.


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The rapid evolution of reproductive genes is well known across many species even if the selective forces pushing these changes are not often obvious. Recently, 285 genes encoding ejaculate in humans, chimpanzees, bonobos and gorillas were analyzed (Good et al., 2013). The hypothesis was that evolutionary rates should be correlated to the intensity of sperm competition. However, this hypothesis was not well supported. Instead they found that the strongest correlation was with effective population size. 4.3. Epigenetics, genomic imprinting and hormones can cause sexual dimorphism in neuroanatomy

Fig. 5. Weighting distribution in cortical as well as subcortical regions found in T1 -weighted gray matter segments (of male and female human brains) included in the multimodal classifier. Left (LH) and right (RH) hemispheres were distinguished and are represented in darker or brighter coloring, respectively. Females had more grey matter vs white matter than male especially in the left hemisphere. The left hemisphere is involved in affiliation, social bonding and empathy. These results show that sexual dimorphism and laterality are important in the evolution of the human brain. From Feis et al. (2013).

4.2. Sexually selected sex differences in gene expression can produce neuroanatomical differences The major histocompatibility complex (MHC) is the one area that has received the most attention for studying the relationship of sexual selection with genomics. The main hypothesis is that through olfactory communication, choice should be for partners with the most dissimilar genes, as this would enhance immune response in offspring (Edwards and Hedrick, 1998). The supposed effects are wide ranging, including avoiding consanguineous breeding through dispersal. These hypotheses have been tested in both human and non-human primates (Grammer et al., 2005). Setchell and Huchard (2010) concluded that MHC dependent mate choice occurs across the primate order. But in reality the record is spotty. For example some support has been found in humans, lemurs and mandrills, but no correlations were found in baboons and macaques (Huchard et al., 2013; Huchard et al., 2010; Huchard and Pechouskova, 2014; Schwensow et al., 2008; Setchell et al., 2013). Due to technical difficulties, the interplay between sexual selection and reproduction in maintaining MHC polymorphisms is not entirely clear (Huchard and Pechouskova, 2014). Homeobox genes are genes that are involved in the regulation of morphogenesis; they mostly act as transcription factors that switch on cascades of other genes. Homeobox genes are normally highly conserved, but there are a few cases of rapid evolution and copy number changes. RHOXF2 (Rhox homeobox family, member 2), an X-linked gene highly expressed in testes and brains, is one such case in primates. Recently Niu et al. (2011) compared humans with 16 non-human primate species for this gene as well as the expression patterns. Significant variation was found in copy number. Most (11) primate species have one copy, while humans and Old World monkeys have two copies and the chimpanzee has six copies. Humans were unique in that they have homogenized their two RHOXF2 copies through recombination. Phylogenomic analysis indicates strong positive selection especially in humans and chimpanzees. Sexual selection acting on the male reproductive system probably drove rapid evolution in RHOXF2 (Niu et al., 2011), but this hypothesis needs further testing.

Epigenetic phenomena apparently influence morphology, brain and behavior (Jaˇsarevic´ et al., 2012). An emerging field of research is the epigenetic of sexually selected traits. In this case Shi et al. (2014) recently compared humans, apes and Old World monkeys and showed that epigenetic regulation through methylation was significantly reduced in humans for four microcephaly genes. The larger neural progenitor pool probably contributed to the dramatically enlarged human brain and cognitive skills associated with human evolution. Genomic imprinting also appears to be important in sexual selection (Wilkins and Haig, 2003). Genomic imprinting leads to parental specific gene expression and is a special case of epigenetics which involves DNA methylation and histone modification. It is generally thought that females can manipulate genomic imprinting during gestation at the detriment of the father’s genome. Imprinting would seem to be the natural outcome of conflicting reproductive strategies as predicted by sexual selection theory. In this case the phenomena would appear to favor females as it can be interpreted to represent a special case of female cryptic selection favoring female choice. However, the full implications of imprinting for sexual selection are a field of research waiting to be explored. The best known mechanisms of epigenetic regulation are those triggered by exposure to steroid hormones. The hypothesis is that these hormones influence expression pathways through DNA methylation, histone protein alterations, and even changes of noncoding RNA. Rimol et al. (2010) showed that common variants of MCPH genes accounted for variation in both normal and diseased human brains. Significantly, they found that there were sex-specific associations with brain volume and cortical surface areas. Only men were negatively affected and they hypothesized that this difference was due to hormonal differences between sexes during early embryonic development. Paus (2010) found a clear difference in an adolescent sample (12–18 years of age); white matter density was greater in females than in males. Apparently, rising levels of testosterone contributed to a decrease in white matter in male adolescents. Treatment of female and male transexuals with hormones was shown to provoke changes in neuroanatomy (Rametti et al., 2012; Zubiaurre-Elorza et al., 2014). 4.4. Social environment influences differences in neuroanatomy between males and females There is additional supporting evidence for the influence of gene expression and epigenetic effects on neuroanatomy and function from non-primate animal models. Data from animal models should be informative because, if these processes have meaningful effects on the brain in these animals, they should be important for primates including humans. Bailey and Moore (2012) recently showed how female choice is often flexible according to the social environment in which they are expressed. The genetic effects are indirect, but can influence the rate and direction of evolutionary change. Sexual selection models often have difficulty capturing the dynamics, but indirect genetic effects can cause rapid sexual trait divergence, including runaway exaggerated traits through

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social feedback (Bailey and Moore, 2012). Female choice can be manifested through sexual imprinting, mate choice, copying and learning. They conclude that the social environment is one of the most important sources of environmental variation for organisms. These variables were tested in insects but are probably even more important in social mammals such as primates. Cummings (2012) recently reviewed these mechanisms in poeciliid fishes. Candidate genes were associated with female preferences and genomic pathways underlying female social interactions with males. Importantly, the networks were positively correlated with female choice, but inhibited in coercive species. Female preferences exhibit a learned component because synaptic connections are modulated and connections are reinforced as females assess males. These genes are highly conserved across vertebrates. This mechanism probably functions in primates since there is behavioral evidence of experience-dependent mate choice across taxa from fish to birds and mammals (Cummings, 2012). So we have come full circle in a feedback system that links genes, gene expression, hormones, morphology, social structure and behavior. Research shows that human sex differences in neuroanatomy may be influenced by socialization. For instance, the white matter microstructure in female-to-male transsexuals differed from those in females, but not from that in males (Rametti et al., 2012). It may prove difficult to isolate the effects of sexual selection from other influences on neuroanatomy. But it may be noted that testosterone levels are often associated with male competition, aggression and coercion (Book et al., 2001; Mehta and Beer, 2010). Perhaps an additional hypothesis is warranted. It is likely that coercive males do not provide a social environment that facilitates the evolution of intelligence even when the potential exists. Lower male competition and increasing female choice may be a necessary initial step in releasing neuroanatomical potential for the entire species. Human evolution is the most dramatic case. If the hypothesis is correct then probably the expansion of human cognitive capacity was accompanied by a lowering of male competition and an increase in female choice. 5. A scenario of human evolution linking sexual selection, behavior, social structure, gene expression and neuroanatomy We can now appreciate that a feedback system links behavior, social organization, mating patterns, and gene expression to sexual dimorphism: from the form and function of the genitalia, to neuroanatomy and the genome. It is possible to develop hypotheses about the interaction of these factors in the evolution of our own species. 5.1. Uniqueness of human reproductive anatomy Human male reproductive anatomy is strikingly different from that of other primates. Human males lack the os penis (baculum) found in all other Old World monkeys and apes. The human penis also has a distinctive coronal ridge and a unique foreskin. The flaccid pars libera length of the gorilla is only 65 mm and that of the orangutan is 85 mm while the length of humans (165 mm), chimpanzees (144 mm) and bonobos (170 mm) is similar (cf Dixson, 2012). However, the penis of both the chimpanzee and bonobo is filiform, ranging from 2 to 4 cm at the base (Dixson and Mundy, 1994a). The circumference of the human penis (average 13.5 cm; Richters et al., 1995) is much larger in comparison with the apes and Old World monkeys making it both relatively and absolutely larger than that found in any great apes species (Dixson, 2012). The larger penis circumference is hypothesized to result from a coevolution with the larger vaginal canal of women, which evolved to permit the passage of larger headed infants (Bowman, 2008). If

this hypothesis is valid it demonstrates an astonishing correlation between the evolution of human neuroanatomy and human genitals. Human testicles on the other hand are less than half that of chimpanzees (Dixson, 2012). Chimpanzee sperm is faster and more vital than human sperm. This is because P. troglodytes sperm show significantly higher mitochondrial membrane potential. Mitochondria provide a substantial part of the energy required for sperm motility (Anderson et al., 2007). Importantly, the genes that are responsible for the unique morphology of the human penis are beginning to be found. Recent research (McLean et al., 2011) shows that in the lineage leading to modern human, males once had small spines on their genitalia such as those found in chimpanzees and other mammals. A comparison of the genomes of humans, chimpanzees and macaques indicates that a DNA sequence thought to play a role in the production of these spines, has been deleted in humans. Rapid evolution has been identified for many reproductive genes and recent studies have combined phylogenetic tests and information on species mating systems to test for the effects of sexual selection on these genes. The molecular evolution of the ADAM (membrane proteins containing A Disintegrin And Metalloprotease domain) gene family is one example (Finn and Civetta, 2010). These proteins act in a highly diverse set of biological processes, including fertilization (sperm–egg adhesion) and neurogenesis. It is certain that the genomic changes associated with other aspects of human male reproductive anatomy will soon be forthcoming. Adult human females also have unique reproductive characteristics: they lack estrus and have permanently swollen breasts. Concelaed estrus in humans – and also in bonobos – is linked to more equilibrated male–female relationships. The lack of estrus is often explained as a strategy to maximize female choice by avoiding male coercion to mate. The swollen breasts of human females may be a substitute of the estrus swellings found in many Old World monkeys and apes. It is thought that sexual signaling moved to the front as our hominid ancestor assumed an erect posture and bipedalism (Gallup, 1982; Mascia-Lees et al., 1986). An analogous transition occurred in the Hamadryas baboon. These monkeys spend most of their time sitting down as they browse grasses on the high Ethiopian plains. To make more visible, their sexual signaling has moved from the anal/genital area to the chest where bright red sexual skin is found today. The most important hypothesis is that the permanently swollen human breasts function as ornaments. 5.2. Sexual selection drove a clear trend toward pair bonding and increased paternal investment Ornamental breasts must have evolved through increased competition among females for males. Ornaments are evidence that the investment of the other sex is a limiting resource, important for the survival of offspring. It is hard to escape the conclusion that breasts are sexually selected and are used by males to choose mates. Body fat deposition on the breasts and hips also appear to have been shaped at least in part by male mate choice (Puts, 2010). This is an example of how sexual selection theory can aid in explaining the unique features of human reproductive anatomy. The differences can best be explained by a trend toward pair bonding and a more monogamous mating system. In this case female competition over mates will be stronger under pair bonding so females needed to evolve ornaments as extravagant as those more commonly seen in males (Clutton-Brock and Huchard, 2013). This trend also explains the loss of estrus in humans. In many Old World primates the size of swellings is consistent with cycles: making swellings a good indicator of fertility. Given that chimpanzee males are likely to be physically stronger and dominant over


females, this common situation can lead to male coercion negating female choice. Concealed estrus in humans – and also in bonobos – is linked to more balanced male–female relationships. The lack of concealed ovulation is often explained as a strategy to maximize female choice by avoiding male coercion to mate, although bonobos and humans resort to different strategies. Humans have eliminated the outward signs of estrus and ovulation, whereas bonobos maintain a prolonged turgid swelling that equally masks female cycles (Fig. 3). In both species female choice has become the winning strategy. A collateral effect is to drastically lower male competition in both species. In bonobos, females forge tight bonds with other females and are dominant over males, a highly unusual situation in Old World primates. Male dominance may be the official norm in the majority of modern human cultures, but clearly female roles are highly influenced by cultural variables making it difficult to trace the evolution of dominance structure in our species. However, we can still conclude that concealed ovulation has lowered human male–male competition (Marlowe and Berbesque, 2012) allowing increased female choice. A trend toward monogamy is characterized by an increase in paternal investment and prolonged pair bonding. Under this scenario hominid females need to attract, choose and retain males for provisioning. When both parents provide considerable care or investment in offspring both sexes must optimize their reproductive success by choosing the best possible mate. Human males are therefore expected to be increasingly more selective about their partners as the trend toward pair bonding intensifies. Developmental differences in the hominid face of males and females, not explained by size difference, were attributed to sexual selection. The relative shortening in men and lengthening in women of the anterior upper face at puberty is the mechanistic consequence of extreme maxillary rotation during ontogeny. Other traits are apparently under mate choice control (Verweij et al., 2014). McLean et al. (2011) proposed that the loss of spines in humans, might be related to human courtship and pair bonding. The loss of spines, they say, would result in less sensitivity and longer copulation, and may be associated with stronger pair bonding in humans resulting in greater paternal care for human offspring. The relatively large length of the human penis may also be subject to female choice. Surprisingly, larger penis size and greater height had almost equivalent positive effects on male attractiveness. Female mate choice could have driven the evolution of larger penises in humans (Mautz et al., 2013). Orgasm in human females may have evolved to consolidate pair bonding, but there is a long-standing discussion even about the existence of female orgasm in non-human primates. However, many physiological components of orgasm are found in non-human primates including macaques, gorillas, chimpanzees and bonobos. The existence of orgasm in these species seems likely and may also promote conception (Puts et al., 2012). In humans contrasting positions view female orgasm as a by-product of male orgasm or as an adaptation, a directly selected characteristic through mate-choice. Further, in non-human primates female orgasm is more frequent with high ranking than low ranking males (Troisi and Carosi, 1998). The high variability in female orgasm frequency and clitoral length suggests that selection for female orgasm is relatively weak. However, this variability may also motivate women to copulate longer to active orgasm and repeatedly with males, which are “good” at sex or have high social value (Puts et al., 2012). This suite of characteristics would promote pleasure, bonding with males who should then invest more in eventual offspring. Selection pressure may then influence both male and female traits, which promote orgasm during copulation. The subsequent pair bonding could then operate in humans to reduce sexual dimorphism and canine size, sperm competition and testes size and in general male competition for mates (Puts et al., 2012).

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Fig. 6. This bar graph shows the percent difference of male to female body size in a series of fossil hominids, from the most ancient to modern humans. From left to right Australopithecus anamensis, A. afarensis, A. africanus, Homo habilis, H. rudolfensis, H. erectus, H. neanderthalensis and H. sapiens. Note that sexual dimorphism drops considerably with the evolution of the genus Homo. Data are from Fleagle (2013).

5.3. Decrease of sexual dimorphism in the genus Homo is evidence of increased female choice and decreased male competition The reduction of sexual dimorphism during the evolution of the human line is good material evidence in support of the trend toward pair bonding and monogamy. Paleoanthropologists have long noted a reduction in sexual dimorphism in the human line (McHenry, 1992) and the decreasing degree of sexual dimorphism has been used as a criterion of hominization through time. It seems very likely that this trend is the result of a change in mating patterns, a tendency to less polygynous relationships in the human line (Plavcan, 2003). Our knowledge from comparative studies in primates strongly supports this claim. Exactly when the decrease in sexual dimorphism began and reached modern levels of variability is uncertain, but the general view is that dimorphism was more extreme in pre-Homo species and that it is lower in the genus Homo (Larsen, 2003). A recent report showing that early members of the genus Homo still maintained high levels of sexual dimorphism even after their exit from Africa (Lordkipanidze et al., 2013) supports the view that the trend toward lower dimorphism continued at least until the appearance of modern humans (Fig. 6). 5.4. The neuroanatomy of pair-bonding and stable social system in the human lineage One of the most dramatic tissue expansions in human evolution is the increased size of the cerebral cortex. Many genomic changes have been discovered over the last few years, which promote the increase of brain size in our lineage (McLean et al., 2011; Sherwood et al., 2008). Lindenfors et al. (2007) have shown that brain structures have developed differently in primate males and females due to divergent pressures on the sexes and to keep up with social cooperation or competitive aggression. It is possible to conclude that, in the transition from promiscuity to pair bonding (Gavrilets, 2012), the high investment required from both parents in offspring requires greater social acuity and abilities to detect cheating. Sexual selection may help explain the expansion of the prefrontal cortex, which mediates important components of complex social behavior such as planning, working memory and language. This scenario would be in compliance with the social brain hypothesis (Dunbar, 2009). The relationship between brain size and the complex neuroanatomy needed to support pair bonding is part of a feedback mechanism. As the brain of Homo increased, brain development

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after gestation became ever more important leaving the young increasingly dependent on provisioning with highly nutritious, protein-rich foods. The demands of children cannot be adequately met solely by the mother. These needs could best be guaranteed by more stable pair bonding. An increasing importance of provisioning for altricial young would selectively reward provisioning males. Thus pair bonding and increasing brain size are certainly an adaptive complex. It is now becoming a general conclusion that transition to long-term pair bonding was a crucial tendency in human evolution (Walum et al., 2012). Stable pair bonding would be a necessary first step in the social structure recently proposed for hunter-gatherers (Hill et al., 2011). Compared to other primates, hunter-gatherers have a unique social structure. It is often assumed that human social structure must have evolved from the fusion-fission system found today in chimpanzees and bonobos. However, we cannot be certain if the social system of the bonobo or chimpanzee or even something intermediate represents the basal condition of the human lineage. It may be that the fusion–fission system evolved in a common ancestor of these apes after the divergence of humans and is a derived behavior trait linking these two Pan species. Human evolution from a multimale–multifemale system such as that found in many Old World monkeys may be just as plausible and perhaps a better model. Chapais (2013) has recently outlined why the distinctive characteristics of human social groups more likely derived from the multimale–multifemale system. Human societies can be considered federations of multifamily groups. These groups resemble multimale–multifemale groups found in other primates with the addition of stable male–female bonding. Hunter-gatherers bands may have individuals, which are not connected by either kinship or marriage ties, yet include males with a vested interest in the offspring of daughters, sisters and wives. Hill et al. (2011) summarized other particular features of human societies: (i) either sex may disperse or remain in their natal group, (ii) adult brothers and sisters often co-reside, and (iii) many individuals in residential groups are genetically unrelated. The differences between human societies is probably based both on historical and ecological variables, but all can be considered as cooperative breeding units. This view is supported by a recent survey of literature from 45 human societies, which shows that often individuals in the maternal line provide crucial aid especially when the contribution of the father is low (Sear and Mace, 2008). All human societies have multilayer complexity, high coordination and an extensive domain of formal kinship recognition, which often operates as a collective form of mate selection. Clearly, human social structure facilitates the interactions and connections with a much higher number of individuals than any other primate species. Hunter-gatherer groups are noted for having 400 times lower lethal aggressive interactions compared to chimpanzees (Wrangham et al., 2006). Lower aggression would facilitate interaction and the development of large social networks. Therefore the lowered male competition that evolved under pair bonding was a fundamental change necessary for the development of human society. These larger social networks may help to explain why humans evolved exponential capacities for social learning that resulted in cumulative culture. This quantum leap permitted a much higher demographic potential compared to our closest relatives, the great apes, and probably lies at the basis of our capacity to expand over the face of the globe.

6. Conclusions Without doubt Darwin’s theory of sexual selection (1871) reflected common Victorian biases. Nevertheless, the hypothesized

continuity from non-human and human primates (pp 105–106), still represents a current and controversial topic: “(. . .) the difference in mind between man and the higher animals, great as it is, is certainly one of degree and not of kind. (. . .) I will make some few remarks on the probable steps and means by which the several mental and moral faculties of man have been gradually evolved”. Darwin restricted the effects of sexual selection primarily to males, especially male ornaments and armaments, and used it to account for racial differences such as skin color and intelligence. It is now appreciated that environmental variables may account for skin color and that sex-dimorphic traits in behavior, genital morphology, reproductive proteins and gene expression can be molded by sexual selection. Both females and males compete and can both increase fitness through the choice of superior partners. Similar selection drives operate in both sexes and differences may be quantitative rather than qualitative (Clutton-Brock and Huchard, 2013). A good argument can be made that strong pair bonding accompanied by relaxed male competition was an essential step in human evolution (Bribiescas et al., 2012). It permitted an increased investment in offspring and many of the defining life history traits of our species including the development of human society. It is clear that the characters shaped by sexual selection are an intimate part of what it means to be human and so they constitute a legitimate, integral part of anthropological investigation. It is important to understand the history of sexual selection theory, because with its eclipse in the first half of the 20th century virtually all anthropological, social and psychological sciences developed without recognizing that sexual selection influenced the evolution of the human body, mind and culture. It is equally clear that the mechanisms underlying sexual selection and the traits associated with them are both more diverse and more complex than initially realized and may be a part of a feedback mechanism. Fortunately, methods have also greatly improved. Of particular interest are molecular tools, which now allow the phenotype subject to sexual and social selection to be linked to the genome.

Acknowledgements Funding was provided by a grant from the University of Florence to RS. The authors thank E. Palagi for the photograph of bonobo swellings and M. Svartman for comments. The authors also thank the reviewers and the editors in particular L. Beani for essential points in revision of this paper.

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Sexual selection and the adaptive evolution of PKDREJ protein in primates and rodents.

Rapid evolution of BRCA1 and BRCA2 in humans and other primates.

Sexual selection and MHC genes.

Sexual selection in gallus: Effects of morphology and dominance on female spatial behavior.

The evolution of female sexuality and mate selection in humans.

Complexity, Natural Selection and the Evolution of Life and Humans.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids.

Evolution of the central sulcus morphology in primates.

Pheromone evolution and sexual behavior in Drosophila are shaped by male sensory exploitation of other males.

Morphology of olfactory epithelium in humans and other vertebrates.

Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana.

Mating, sexual selection, and the evolution of schizophrenia.

The role of DNA insertions in phenotypic differentiation between humans and other primates.

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology.

Postsacral vertebral morphology in relation to tail length among primates and other mammals.

Multiple sexual selection pressures drive the rapid evolution of complex morphology in a male secondary genital structure.

Hormonal steroids and sexual communication in primates.

'Concealed ovulation' and sexual signals in primates.

The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae).

Masculine sexual behavior and morphology: paradoxical effects of perinatal androgen treatment in male and female rats.

Plant size, sexual selection, and the evolution of protandry in dioecious plants.

Rapid evolution of the cerebellum in humans and other great apes.

An Exceptional Gene: Evolution of the TSPY Gene Family in Humans and Other Great Apes.

AIDS and other STDs in Carriacou.