The relative importance of intra- and intersexual selection on human male sexually dimorphic traits

Recent evidence suggests that in sexual selection on human males, intrasexual competition plays a larger role than female choice. In a sample of men (N?=?164), we sought to provide further evidence on the effects of men's physical dominance and sexual attractiveness on mating success and hence in sexual selection. Objective measures and subjective ratings of male sexually dimorphic traits purportedly under sexual selection (height, vocal and facial masculinity, upper body size from 3D scans, physical strength, and baseline testosterone) and observer perceptions of physical dominance and sexual attractiveness based on self-presentation video recordings were assessed and associated with mating success (sociosexual behaviour and number of potential conceptions) in a partly longitudinal design. Results from structural equation models and selection analyses revealed that physical dominance, but not sexual attractiveness, predicted mating success. Physical dominance mediated associations of upper body size, physical strength, as well as vocal and facial physical dominance and attractiveness with mating success. These findings thus suggest a greater importance of intrasexual competition than female choice in human male sexual selection.     

Male voice pitch mediates the relationship between objective and perceived formidability

Acoustic signals function in intrasexual mating competition in a wide variety of species, including humans. The low voice pitch of human males has been proposed to represent an honest signal of formidability. Although voice pitch in men affects perceptions of size and dominance, it is relatively weakly associated with objective measures of formidability such as body size and strength. As a result, some authors have argued that low male voice pitch is not a valid signal of formidability but is deceptive and salient only because it hijacks a tendency to perceive lower frequency sounds as emanating from larger sources. In this paper, we consider theoretical and empirical issues associated with this perceptual exploitation hypothesis and ask whether male voice pitch transmits information about formidability. We utilize mediation models to investigate whether male voice pitch is an honest signal of formidability in data collected from university students in the U.S. (n = 231 male speakers, 565 male raters) and Canada (n = 74 male speakers, 108 female raters, 65 male raters). In both data sets, male voice pitch mediated the relationship between objective (measured by height) and perceived formidability. Collectively, these results indicate that men’s voice pitch transmits information about formidability from signaler to receiver.     

Beauty and the beast: mechanisms of sexual selection in humans

Literature in evolutionary psychology suggests that mate choice has been the primary mechanism of sexual selection in humans, but this conclusion conforms neither to theoretical predictions nor available evidence. Contests override other mechanisms of sexual selection; that is, when individuals can exclude their competitors by force or threat of force, mate choice, sperm competition, and other mechanisms are impossible. Mates are easier to monopolize in two dimensional mating environments, such as land, than in three-dimensional environments, such as air, water, and trees. Thus, two-dimensional mating environments may tend to favor the evolution of contests. The two-dimensionality of the human mating environment, along with phylogeny, the spatial and temporal clustering of mates and competitors, and anatomical considerations, predict that contest competition should have been the primary mechanism of sexual selection in men. A functional analysis supports this prediction. Men's traits are better designed for contest competition than for other sexual selection mechanisms; size, muscularity, strength, aggression, and the manufacture and use of weapons probably helped ancestral males win contests directly, and deep voices and facial hair signal dominance more effectively than they increase attractiveness. However, male monopolization of females was imperfect, and female mate choice, sperm competition, and sexual coercion also likely shaped men's traits. In contrast, male mate choice was probably central in women's mating competition because ancestral females could not constrain the choices of larger and more aggressive males through force, and attractive women could obtain greater male investment. Neotenous female features and body fat deposition on the breasts and hips appear to have been shaped by male mate choice.     

Young,formidable men show greater sensitivity to facial cues of dominance

There is considerable evidence that human male faces contain honest, detectable cues to their physical dominance, which are related to their objective facial masculinity. As such, some have argued that the extent to which observers' rate masculinised male faces as appearing more physically dominant is a useful measure of their ability to detect cues of dominance and threat in other men. We found across 3 studies (total n = 272) that younger, taller, and stronger men showed greater sensitivity to facial cues of dominance. Additionally, participants were more likely to associate younger than older masculinised faces with physical dominance. Self-perceived social dominance did not moderate perceptions. These results contrast with previous work which found that shorter, less socially dominant men had greater ability to detect facial cues of dominance. We propose the hypothesis that younger, more formidable males show greater sensitivity to facial cues of dominance as they are more likely to engage in violent intrasexual competition.     

Aggression in young men high in threat potential increases after hearing low-pitched male voices: two tests of the retaliation-cost model

Research suggests that male voice pitch is an honest dominance signal because it indexes men's physicality and because lower-pitched voices are more costly to develop and maintain. Rather than considering these signaler-dependent mechanisms, we tested a receiver-dependent mechanism hypothesized by M. Enquist's (1985) retaliation-cost model of aggressive signaling. The model predicts that, given a competitive scenario, low-pitched male voices will elicit aggression from male listeners (i.e., signal receivers) who are relatively high in threat potential. We confirmed this hypothesis in two experiments. Under a sexual but not control prime and after listening to low- but not average-pitched male voices, increases in heterosexual male participants' trait dominance predicted stronger aggressive cognitions (Experiment 1), and increases in male participants' handgrip strength predicted stronger aggressive intent (Experiment 2). These findings provide the first direct support for the retaliation-cost model in humans, extend research on the effects of male voice pitch on receiver psychology, and demonstrate an additional cost mechanism that explains why voice pitch is an honest signal of dominance in men.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male-male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male-male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid-based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male-male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.     

Pitch lowering enhances men's perceived aggressive intent,not fighting ability

Voice pitch is the primary perceptual correlate of fundamental frequency (f_o) and describes how low or high a voice is perceived by listeners. Prior research showed that men whose habitual voice pitch is lower are perceived to have stronger fighting ability. However, voice pitch is also flexible and can thus be used facultatively to signal states that change situationally, such as current aggressive intent (i.e., readiness to use aggression). Drawing on motivation-structural-rules theory, this research tests the hypothesis that male speakers will be perceived as more likely to attack when they lower (compared to raise) their pitch to address an adversary in a conflict situation. Three experiments using male speakers and listeners supported this hypothesis, both with and without controlling for the perception of the speakers' fighting ability. In contrast, the same experiments found no evidence that pitch lowering enhanced the speakers' perceived fighting ability after controlling for their perceived aggressive intent. Moreover, we found mixed evidence that the speakers' perceived physical strength interacted with pitch modulation to influence their perceived aggressive intent. On balance, these findings show that, at least for men, pitch modulation is primarily an aggressive-intent signal assessed independently of signalers' fighting ability. Future research should distinguish between perceptions of aggressive-intent and fighting-ability when examining the perceptual effects of male voice-pitch modulation in intrasexual competition.     

Sexual Selection in Black Morph Girardinus metallicus (Pisces: Poeciliidae): Females Can Spot a Winner (But We Cannot)

Male–male competition may interfere with the ability of females to choose mates by interrupting courtship or by favoring highly aggressive males who may damage females during mating attempts. Alternatively, females may benefit by mating with dominant males, and female choice and male–male competition may therefore act in unison. The same traits, including aggressiveness, may indicate male quality to females and to rivals. We investigated sexual selection in the black morph of the endemic Cuban poeciliid fish, Girardinus metallicus, to ascertain the links between morphological and behavioral traits and success in intra‐ and intersexual selection. Males conspicuously exhibit their black ventral surface and gonopodium to females during courtship. Dichotomous choice tests revealed female association preferences for certain males, and those same males were more successful in monopolizing access to females when the fish were allowed to directly interact. Dominant males followed, courted, and copulated with females more than subordinate males within a pair, and it appears that females could either assess dominance based on cues we did not measure, or could influence subsequent mating success by their behavior during the dichotomous choice trials. There was an interaction between black status (i.e., whether the male in each pair had more or less ventral black coloration than the other male in that pair) and dominance, such that low‐black dominant males courted early and then shifted to following females, whereas high‐black dominant males courted far more later in the observation period. These results hint at the importance for sexual selection of the interplay between a static morphological trait (black coloration) and a dynamic behavioral trait (aggressiveness), but the functional significance of the courtship display remains a mystery.     

Quantifying the strength and form of sexual selection on men's traits

Although recent research has increasingly focused on human sexual selection, fundamental questions remain concerning the relative influence of individual traits on success in competition for mates and the mechanisms, form, and direction of these sexual selective pressures. Here, we explore sexual selection on men's traits by ascertaining men's dominance and attractiveness from male and female acquaintances. On a large American university campus, 63 men from two social fraternities provided anthropometric measurements, facial photographs, voice recordings, and reported mating success (number of sexual partners). These men also assessed each other's dominance, and 72 women from two socially affiliated sororities assessed the men's attractiveness. We measured facial masculinity from inter-landmark distances and vocal masculinity from acoustic parameters. We additionally obtained facial and vocal attractiveness and dominance ratings from unfamiliar observers. Results indicate that dominance and the traits associated with it predict men's mating success, but attractiveness and the traits associated with it do not. These findings point to the salience of contest competition on men's mating success in this population.     

Preference for Leaders with Masculine Voices Holds in the Case of Feminine Leadership Roles

Human voice pitch research has focused on perceptions of attractiveness, strength, and social dominance. Here we examine the influence of pitch on selection of leaders, and whether this influence varies by leadership role. Male and female leaders with lower-pitched (i.e., masculine) voices are generally preferred by both men and women. We asked whether this preference shifts to favor higher-pitch (i.e., feminine) voices within the specific context of leadership positions that are typically held by women (i.e., feminine leadership roles). In hypothetical elections for two such positions, men and women listened to pairs of male and female voices that differed only in pitch, and were asked which of each pair they would vote for. As in previous studies, men and women preferred female candidates with masculine voices. Likewise, men preferred men with masculine voices. Women, however, did not discriminate between male voices. Overall, contrary to research showing that perceptions of voice pitch can be influenced by social context, these results suggest that the influence of voice pitch on perceptions of leadership capacity is largely consistent across different domains of leadership.     

Elevated recognition accuracy for low-pitched male voices in men with higher threat potential: Further evidence for the retaliation-cost model in humans

For humans, voice pitch is highly flexible and, when lowered, makes male speakers sound more dominant, intimidating, threatening, and likely to aggress. Importantly, pitch lowering could not have evolved as a threat signal with these effects on signal receivers unless it were honest on average. Drawing on Enquist's retaliation-cost model, we tested the hypothesis that heterosexual men high in threat potential will show enhanced memory for low-pitched male voices when mating motives were activated. Supporting this hypothesis, we found that heterosexual Chinese males higher in trait aggressiveness (Experiment 1) and heterosexual U.S. males higher in upper-body strength (Experiment 2) were more accurate in distinguishing between previously heard and unheard low- but not high-pitched male voices under a mating-motive prime. We believe that this enhanced recognition accuracy for low-pitched male voices facilitates retaliation for men with high threat potential, and thereby serves to probe the honesty of pitch lowering as an aggressive signal.     

Female lizards ignore the sweet scent of success: Male characteristics implicated in female mate preference

Sexual selection molds the morphology, physiology and behavior of males in many animals. At first glance, it seems reasonable to assume that females would use the same male traits and signals in mate choice as males do during male-male competition. However, intra- and intersexual competition may affect traits in the same or the opposite direction, with differing strength. We investigated which color, morphometric and performance traits are selected for through male-male competition and whether female mate preference is based on these same traits and/or dominance status in the three male color morphs of the lizard Podarcis melisellensis. Males with relatively bigger heads and relatively higher bite forces were more likely to win fights and orange males were always dominant over the other morphs. Females, however, preferred scents of bigger males that were in better body condition, and surprisingly had lower bite force capacities. They did not show a preference for scents of any particular color morph or for scents of the more dominant males. These results indicate that intra- and intersexual competition may result in selection for different secondary sexual traits in P. melisellensis.     

`Little Chipmunk' Syndrome? Male Body Size and Dominance in Captive Yellow‐Pine Chipmunks (Tamias amoenus)

In mammals, large males are often assumed to have higher mating success because they have greater success at contest competition. This relationship is often used to explain the prevalence of male-biased sexual size dimorphism in mammals. However, in many small vertebrates, large individuals are not always dominant. Using staged dyadic encounters, we examined the relationship between male body size and social dominance in captive male yellow-pine chipmunks ( Tamias amoenus ), a species with female-biased sexual size dimorphism. The yellow-pine chipmunk has a mating system in which males participate in mating chases and dominant males may have an advantage in acquiring matings with oestrous females. Captive male chipmunks were aggressive in only 28% of 144 paired encounters; however, several lines of evidence indicated that smaller chipmunks were dominant over large chipmunks: (1) small males were dominant in more dyads than large males; (2) within dyads, dominant males were smaller than subordinate males; and (3) small males performed more aggressive behaviour than large males. These results are not consistent with the prediction that large males are typically dominant. If large chipmunks are able to gain matings with females because of qualities other than dominance (such as the ability to successfully find and/or chase receptive females), then the costs of aggression to large chipmunks may outweigh any potential benefits. Small males, but not large males, may improve their mating success by being aggressive.     

Effects of partner conception risk phase on male perception of dominance in faces

Several studies have suggested that women may prefer to engage in extra-pair copulations with males who appear dominant and to do so near ovulation. While there is some evidence that males are more jealous of dominant rivals and more proprietary when their partners are near ovulation, there is none that suggests the existence of counterstrategic perceptual shifts that mirror those seen in women. We provide such evidence here. Composites of male faces that were either high or low in rated dominance were presented to male participants who provided ratings of dominance. A three-way interaction between stimulus-face dominance, partner conception risk phase, and partner oral contraceptive use was found; men whose partners did not use an oral contraceptive and were in the high conception risk phase of their cycle displayed increased dominance ratings of high-dominance male faces. We conclude that males have evolved counterstrategies to deal with female infidelity that include an overattribution of dominance to those rivals most likely to present a threat at times when that threat is greatest. This overattribution is likely to lead to increases in jealousy and mate-retention behaviors.     

Sexual selection for low male voice pitch among Amazonian forager-horticulturists

Pitch is the most perceptually salient feature of the voice, yet it is approximately five standard deviations lower in men than in women, a degree of sexual dimorphism exceeding that of all extant nonhuman apes. Evidence from Western samples suggests that low-frequency vocalizations may have augmented male mating success ancestrally by intimidating competitors and/or attracting mates. However, data are lacking from small-scale societies. We therefore investigated sexual selection on male pitch (measured by fundamental frequency, f_o) in a population of Bolivian forager-horticulturists, the Tsimané. We found that experimentally lowering f_o in audio clips of men speaking increased perceptions of fighting ability but did not affect perceptions of prestige and decreased their attractiveness to women. Further, men with lower speaking f_o reported higher numbers of offspring, and this was mediated by the reproductive rates of men's wives, suggesting that men with lower f_o achieved higher reproductive success by having access to more fertile mates. These results thus provide new evidence that men's f_o has been shaped by intrasexual competition.     

Are men better than women at acoustic size judgements?

Formants are important phonetic elements of human speech that are also used by humans and non-human mammals to assess the body size of potential mates and rivals. As a consequence, it has been suggested that formant perception, which is crucial for speech perception, may have evolved through sexual selection. Somewhat surprisingly, though, no previous studies have examined whether sexes differ in their ability to use formants for size evaluation. Here, we investigated whether men and women differ in their ability to use the formant frequency spacing of synthetic vocal stimuli to make auditory size judgements over a wide range of fundamental frequencies (the main determinant of vocal pitch). Our results reveal that men are significantly better than women at comparing the apparent size of stimuli, and that lower pitch improves the ability of both men and women to perform these acoustic size judgements. These findings constitute the first demonstration of a sex difference in formant perception, and lend support to the idea that acoustic size normalization, a crucial prerequisite for speech perception, may have been sexually selected through male competition. We also provide the first evidence that vocalizations with relatively low pitch improve the perception of size-related formant information.     

Male–Male Competition in a Mixed‐Mating Fish

Mating systems that comprise a mixture of pure males and self‐fertilising hermaphrodites remain an evolutionary enigma. In particular, our understanding of the sexual selection pressures associated with such mating systems is nascent. Males can only reproduce by fertilising hermaphrodites’ eggs, but hermaphrodites can also fertilise their own eggs and gain a genetic advantage by doing so. Consequently, there should be intense competition among males to access hermaphrodites. Here, we test the importance of male size, colour and heterozygosity in predicting the outcome of male–male competition using the mangrove rivulus, which has a male‐hermaphrodite mixed‐mating system. We pitted males against one another in dyadic laboratory trials to develop a dominance score for each male. We then correlated these scores with male length, several components of male colour, and heterozygosity. Male size was the only significant correlate of dominance: larger males dominated smaller males, implying selection for large male size. However, male mangrove rivulus are similar in size to hermaphrodites, indicating that directional selection for large body size in males is no greater than it is in hermaphrodites. Across all trials, colour was unrelated to dominance, but contests between similarly sized males were usually won by more colourful individuals. As mangrove rivulus are dichromatic, we suspect that male colour may prove to be more important in mate choice than we found it to be in intrasexual competition. Heterozygosity did not explain dominance directly, but correlated strongly with male size, implying an indirect role in intrasexual competition.     

Female competition and its evolutionary consequences in mammals

Following Darwin's original insights regarding sexual selection, studies of intrasexual competition have mainly focused on male competition for mates; by contrast, female reproductive competition has received less attention. Here, we review evidence that female mammals compete for both resources and mates in order to secure reproductive benefits. We describe how females compete for resources such as food, nest sites, and protection by means of dominance relationships, territoriality and inter‐group aggression, and by inhibiting the reproduction of other females. We also describe evidence that female mammals compete for mates and consider the ultimate causes of such behaviour, including competition for access to resources provided by mates, sperm limitation and prevention of future resource competition. Our review reveals female competition to be a potentially widespread and significant evolutionary selection pressure among mammals, particularly competition for resources among social species for which most evidence is currently available. We report that female competition is associated with many diverse adaptations, from overtly aggressive behaviour, weaponry, and conspicuous sexual signals to subtle and often complex social behaviour involving olfactory signalling, alliance formation, altruism and spite, and even cases where individuals appear to inhibit their own reproduction. Overall, despite some obvious parallels with male phenotypic traits favoured under sexual selection, it appears that fundamental differences in the reproductive strategies of the sexes (ultimately related to parental investment) commonly lead to contrasting competitive goals and adaptations. Because female adaptations for intrasexual competition are often less conspicuous than those of males, they are generally more challenging to study. In particular, since females often employ competitive strategies that directly influence not only the number but also the quality (survival and reproductive success) of their own offspring, as well as the relative reproductive success of others, a multigenerational view ideally is required to quantify the full extent of variation in female fitness resulting from intrasexual competition. Nonetheless, current evidence indicates that the reproductive success of female mammals can also be highly variable over shorter time scales, with significant reproductive skew related to competitive ability. Whether we choose to describe the outcome of female reproductive competition (competition for mates, for mates controlling resources, or for resources per se) as sexual selection depends on how sexual selection is defined. Considering sexual selection strictly as resulting from differential mating or fertilisation success, the role of female competition for the sperm of preferred (or competitively successful) males appears particularly worthy of more detailed investigation. Broader definitions of sexual selection have recently been proposed to encompass the impact on reproduction of competition for resources other than mates. Although the merits of such definitions are a matter of ongoing debate, our review highlights that understanding the evolutionary causes and consequences of female reproductive competition indeed requires a broader perspective than has traditionally been assumed. We conclude that future research in this field offers much exciting potential to address new and fundamentally important questions relating to social and mating‐system evolution.     

Female preference for dominant males in the Mexican mojarra cichlid fish,Cichlasoma istlanum

It is widely assumed that female preference and male competition operate simultaneously during sexual selection. Dominance is likely an honest indicator of male quality, and females can identify and choose the dominant male to reproduce with individuals with greater competitive abilities, thus improving the quality and competitiveness of their offspring. In this context, few studies have investigated female preference in relation to male fighting ability. The Mexican mojarra, Cichlasoma istlanum, is a cichlid species native to the Balsas River basin. It is territorial during reproduction and provides parental care. Males commonly engage in territorial defence, whereas females care directly for offspring. This study examined whether females prefer dominant males that exhibit more aggressive behaviour. The authors conducted experiments using groups of two males and one female to test competitive ability in males and female preference. They also quantified the time during which the female associated with the dominant male and the subordinate male after observing the outcome of a fight between the two males. They found that Mexican mojarra females preferred dominant males and that the time females spent associating with males was positively related with their aggressive behaviours during competition. These results indicate that dominant males were more attractive than subordinate males to female Mexican mojarra. The relationship between female preference and male dominance in the Mexican mojarra demonstrates the importance of male competitive ability for future parental care in reproduction.