Neuroscience and Biobehavioral Reviews 46 (2014) 579–590

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews

journal homepage: www.elsevier.com/locate/neubiorev

Review

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 a b s t r a c t

Article history: Explaining human evolution means developing hypotheses about the occurrence of sex differences in
Received 27 January 2014 the brain. Neuroanatomy is significantly influenced by sexual selection, involving the cognitive domain
Received in revised form through competition for mates and mate choice. Male neuroanatomy emphasizes subcortical brain areas
20 September 2014
and visual-spatial skills whereas that of females emphasizes the neocortex and social cognitive areas. In
Accepted 1 October 2014
Available online 14 October 2014
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
Keywords:
Sexual dimorphism produce neuroanatomical sex differences. A feedback system links genes, gene expression, hormones,
Social complexity morphology, social structure and behavior. Sex differences, often through female choice, can be rapidly
Female competition modulated by socialization. Human evolution is a dramatic case of how a trend toward pair bonding and
Non-conceptive mating monogamy lowered male competition and increased female choice as a necessary step in releasing the
Brain size cognitive potential of our species.
Epigenetics © 2014 Elsevier Ltd. All rights reserved.
Gene expression

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 580
2. Social structure and mating systems affect body sex-dimorphism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 580
2.1. Female promiscuity and cryptic mate choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 580
2.2. Sperm competition and genitalia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 580
3. Increasing focus on female–female competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 581
3.1. Female secondary sexual characteristic: armaments or ornaments? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 582
4. The impact of sexual selection on primate brains and neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 582
4.1. Gross neuroanatomical differences between sexes: from male competition to female empathy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 583
4.2. Sexually selected sex differences in gene expression can produce neuroanatomical differences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585
4.3. Epigenetics, genomic imprinting and hormones can cause sexual dimorphism in neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585
4.4. Social environment influences differences in neuroanatomy between males and females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585
5. A scenario of human evolution linking sexual selection, behavior, social structure, gene expression and neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . 586
5.1. Uniqueness of human reproductive anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 586
5.2. Sexual selection drove a clear trend toward pair bonding and increased paternal investment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 586
5.3. Decrease of sexual dimorphism in the genus Homo is evidence of increased female choice and decreased male competition . . . . . . . . . . 587
5.4. The neuroanatomy of pair-bonding and stable social system in the human lineage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 587
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 588
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 588
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 588

∗ 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.
580 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 influ-
ence 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 appre-
ciated (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 evo-
lution (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 vari-
ables 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 determin-
ing 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 simpli-
fication are classified as monogamous (pairs), polygynous (one
male with multiple females), polyandrous (one female with multi-
ple 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 dimor-
phism 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 beau-
tiful”; 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 repro-
ductive 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 selec-
tion studies, due to the key role of female mate choice. Rather than
being a cooperative venture between the sexes, sexual reproduc-
tion 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 promis-
cuity, 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 promiscu-
ity 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 max-
imize 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 strate-
gies 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 pri-
mate 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 cor-
relation. 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 func-
tion of larger penises would be both to remove rivals’ sperm
 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590 581

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 relation-
ship of social structure with penis size is not clear-cut. Both
competition and female choice should influence penile mor-
phologies. 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 dur-
ing 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 sex-
ual 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 rela-
tionships 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 con-
clude that mating competition intensity –among males as well as
females – and other parameters of sexual selection – can influ-
ence the group size and the genetic relatedness between group
members.
Female–female competition may consist in a fine social manip-
ulation. 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 sta-
tus 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
582 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590
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) Pri-
mates = 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 maneu-
vers 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 prob-
ably 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 compet-
ing 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, high-
ranking infant survival, faster maturing daughters, and more rapid
production of young are phenomena linked to female competition
(Pusey et al., 1997).
3.1. Female secondary sexual characteristic: armaments or
ornaments?
Female facial coloration has been traditionally viewed as a sex-
ual 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 sec-
ondary 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 suc-
cess (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 lac-
tating 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 pater-
nity 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 behav-
ior 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). Repro-
ductive 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 pri-
mates. We have already seen that there are strong morphological
correlates between mating systems, body and canine dimorphism,
 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590 583

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. Addi-
tionally, 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 com-
petition 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 inher-
ited. 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 evolu-
tion (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 accel-
erated 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. Sex-
dependent 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 dimor-
phism in the brain and neuroanatomy of primates.
Reinius et al. (2008) reported on a conserved sexual genomic sig-
nature 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 liter-
ally hundreds of genes with different expression profiles between
males and females. Many of these genes had higher expression pro-
files 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 expres-
sion. 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 social-
ity is more related to subcortical brain areas whereas that of females
is more related to the neocortex (Lindenfors et al., 2007). These find-
ings 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
584 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590

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 mat-
ter than male especially in the left hemisphere (Fig. 5). The left
hemisphere is involved in affiliation, social bonding and empa-
thy. 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 neu-
roanatomy that controls autonomic functions and sensory-motor
skills as well as those relating to aggression including mesen-
cephalon, 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 discrim-
inated 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 perception-
action mechanism. Mirror neurons are thought to be important in
imitation, learning, empathy and self-awareness. Long standing cir-
cumstantial 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 emo-
tional 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 differ-
ences in mirror neurons were generated by sexual selection in the
brain.
 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590
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 breed-
ing 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 selec-
tion 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 num-
ber. 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 chim-
panzees. Sexual selection acting on the male reproductive system
probably drove rapid evolution in RHOXF2 (Niu et al., 2011), but
this hypothesis needs further testing.
585
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
Epigenetic phenomena apparently influence morphology, brain
and behavior (Jašarević 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 dramat-
ically 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 epigenet-
ics which involves DNA methylation and histone modification. It is
generally thought that females can manipulate genomic imprint-
ing 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 non-
coding 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 differ-
ence 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 ado-
lescents. 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 func-
tion from non-primate animal models. Data from animal models
should be informative because, if these processes have meaning-
ful 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 sex-
ual trait divergence, including runaway exaggerated traits through
586 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590
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 inter-
actions with males. Importantly, the networks were positively
correlated with female choice, but inhibited in coercive species.
Female preferences exhibit a learned component because synap-
tic 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 addi-
tional hypothesis is warranted. It is likely that coercive males do not
provide a social environment that facilitates the evolution of intelli-
gence 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 neu-
roanatomy 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 flac-
cid 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), chim-
panzees (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 gen-
itals. 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. Mitochon-
dria provide a substantial part of the energy required for sperm
motility (Anderson et al., 2007).
Importantly, the genes that are responsible for the unique mor-
phology 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 infor-
mation 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 charac-
teristics: 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 impor-
tant 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 com-
petition 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 chim-
panzee males are likely to be physically stronger and dominant over
 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590
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 main-
tain 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 sce-
nario 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 reproduc-
tive 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. Develop-
mental 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 pos-
itions 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. How-
ever, 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 charac-
teristics 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 dur-
ing copulation. The subsequent pair bonding could then operate in
humans to reduce sexual dimorphism and canine size, sperm com-
petition and testes size and in general male competition for mates
(Puts et al., 2012).
587
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 pat-
terns, 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 vari-
ability 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 sex-
ual dimorphism even after their exit from Africa (Lordkipanidze
et al., 2013) supports the view that the trend toward lower dimor-
phism 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 struc-
tures 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 behav-
ior 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 neu-
roanatomy needed to support pair bonding is part of a feedback
mechanism. As the brain of Homo increased, brain development
588 R. Stanyon, F. Bigoni / Neuroscience and Biobehavioral Reviews 46 (2014) 579–590
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 provi-
sioning 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 evo-
lution 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 char-
acteristics of human social groups more likely derived from the
multimale–multifemale system. Human societies can be consid-
ered 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 off-
spring of daughters, sisters and wives. Hill et al. (2011) summarized
other particular features of human societies: (i) either sex may dis-
perse 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 hav-
ing 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 rela-
tives, 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 ani-
mals, 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 mor-
phology, 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 quan-
titative rather than qualitative (Clutton-Brock and Huchard, 2013).
A good argument can be made that strong pair bonding accom-
panied by relaxed male competition was an essential step in human
evolution (Bribiescas et al., 2012). It permitted an increased invest-
ment 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 sex-
ual 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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