Selective attention toward female secondary sexual color in male rhesus macaques

Pink-to-red anogenital and facial sexual skin occurs in females of many primate species. Since female sexual skin color varies with reproductive state, it has long been assumed that color acts to stimulate male sexual interest. Although there is supportive evidence for this as regards anogenital skin, it is unclear whether this is also the case for facial sexual skin. In this study we experimentally manipulated digital facial and hindquarter images of female rhesus macaques (Macaca mulatta) for color within the natural range of variation. The images were presented to adult male conspecifics to assess whether the males exhibited visual preferences for red vs. non-red female coloration, and whether preferences varied with anatomical region. The males displayed significantly longer gaze durations in response to reddened versions of female hindquarters, but not to reddened versions of faces. This suggests that female facial coloration may serve an alternative purpose to that of attracting males, and that the signal function of sexual skin and the intended recipients may vary across anatomical regions.     

Sexual Skin Color Contains Information About the Timing of the Fertile Phase in Free-ranging <Emphasis Type="Italic">Macaca mulatta</Emphasis>

Females of several primate species undergo cyclical changes of their sexual skin, i.e., the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing.     

SEXUAL SELECTION CAN INCREASE THE EFFECT OF RANDOM GENETIC DRIFT—A QUANTITATIVE GENETIC MODEL OF POLYMORPHISM IN OOPHAGA PUMILIO,THE STRAWBERRY POISON‐DART FROG

The variation in color pattern between populations of the poison‐dart frog Oophaga pumilio across the Bocas del Toro archipelago in Panama is suggested to be due to sexual selection, as two other nonsexually selecting Dendrobatid species found in the same habitat and range do not exhibit this variation. We theoretically test this assertion using a quantitative genetic sexual selection model incorporating aposematic coloration and random drift. We find that sexual selection could cause the observed variation via a novel process we call “coupled drift.” Within our model, for certain parameter values, sexual selection forces frog color to closely follow the evolution of female preference. Any between‐population variation in preference due to genetic drift is passed on to color. If female preference in O. pumilio is strongly affected by drift, whereas color in the nonsexually selecting Dendrobatid species is not, coupled drift will cause increased between‐population phenotypic variation. However, with different parameter values, coupled drift will result in between‐population variation in color being suppressed compared to its neutral value, or in little or no effect. We suggest that coupled drift is a novel theoretical process that could have a role linking sexual selection with speciation both in O. pumilio, and perhaps more generally.     

Steroid correlates of multiple color traits in the spiny lizard, <Emphasis Type="Italic">Sceloporus pyrocephalus</Emphasis>

Conspicuous coloration in females is less well studied compared to that in males. Adult female Mexican boulder spiny lizards (Sceloporus pyrocephalus) have conspicuously colored throat, or gular, regions, ranging from red to yellow, while adult males only weakly express such color in their gular region. Both sexes have dark blue–black gular stripes and venter stripes. Understanding proximate mechanisms underlying trait expression can aid in understanding trait function. To characterize the proximate mechanisms potentially influencing color variation among field-captured male and female S. pyrocephalus, we quantified three aspects of color (hue, saturation, brightness) for three body locations (gular region, gular stripes, venter stripes) and then assessed how color was related to reproductive state and concentrations of the plasma steroid hormones testosterone (T) and corticosterone (CORT) in males and T, CORT, and 17-β estradiol (E₂) in females. Testes volume was not related to variation in color or in hormones, perhaps because most males were in peak reproductive condition. Large vitellogenic follicles as opposed to oviductal eggs were associated with higher E₂ in females. Males with more dull gular stripes and females with dull venter stripes had significantly higher CORT. Females with red gular regions and pale grey gular stripes had higher T and E₂ concentrations compared to females with a more yellow gular region and darker gular stripes. Thus, gular region color in females could communicate reproductive state; dull gular stripes in males and dull venter stripes in females could communicate stress status.     

Sexual Dichromatism and Female Preference in Eulemur fulvus Subspecies

We experimentally tested the hypothesis that sexual dichromatism in the subspecies of Eulemur fulvus is the evolutionary result of female preference for brightly colored males. Ten female lemurs representing 6 different subspecies of Eulemur fulvus were subjects in the experiment; controls were 4 females of non-sexually dichromatic lemurid taxa. For each taxon we presented photographs of the face of a male of that taxon whose colors had been digitally altered to make him less and more colourful. Median viewing times of the pooled female Eulemur fulvus are significantly correlated with colorfulness. Viewing times in the control females are not correlated with color or brightness of the stimulus photographs. We concluded that the females of the Eulemur fulvus sspp. preferred to view photographs of more colorful males, which is consistent with the predictions of sexual selection theory.     

Sexual harassment in a live-bearing fish (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>): influence of population-specific male mating behaviour

We investigated male sexual behaviour and the cost of sexual harassment, as measured by the reduction of female feeding time in the presence of a male, in a cave-dwelling population of Poecilia mexicana, in which sexual harassment does not occur naturally. We asked whether the lack of sexual harassment in this population is due to low sexual activity of the males, or low feeding motivation of the females. We experimentally increased the sexual activity of males or the females feeding motivation, or we used a combination of both treatments. Female feeding time was not lower in the presence of a male than in the presence of a female after sexual deprivation of the males or food deprivation of the females. Only in the combined experiment was female feeding time lower in the presence of a large male than in the presence of a small male, indicating a weak effect of sexual harassment by large males. Virgin females did not suffer a cost of sexual harassment, indicating that sexual experience does not cause the lack of sexual harassment in cave mollies. Males from a surface population, where sexual harassment occurs, significantly reduced the feeding time of cave-dwelling females even though these males exhibited surprisingly little sexual behaviour. The sexual activity of cave mollies did not correlate with male body size in any experiment, indicating that even after sexual deprivation, small cave molly males do not switch to the alternative mating behaviour known in surface-dwelling P. mexicana, where sexual activity is correlated negatively with male body size.     

Sexual behavior in brown capuchins ( Cebus apella )

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Males,but not females,contribute to sexual isolation between two sympatric species of <Emphasis Type="Italic">Gambusia</Emphasis>

Reproductive isolation restricts genetic exchange between species. Various pre- and post-mating barriers, such as behavior, physiology and gametic incompatibility, have been shown to evolve in sympatry. In certain scenarios, isolation can be asymmetrical, where species differentially prefer conspecifics. We examined sexual isolation via conspecific mate preference between Gambusia affinis and G. geiseri in both sexes. To investigate male contribution to sexual isolation, we compared the number of mating attempts (gonopodial thrusts) directed at either a conspecific or a heterospecific female, in both species. We also examined sperm priming and expenditure in males in the presence of conspecific or heterospecific females. We then measured female preference for either a conspecific or heterospecific male, in both species. We found that males of both species preferred to mate with conspecific females, but showed no difference in sperm production or expenditure between conspecific and heterospecific females. Females of both species did not prefer conspecific over heterospecific males. Our results suggest that sexual isolation might be mediated by male mate choice in this system and not female choice, suggesting that there is asymmetrical reproductive isolation between the sexes in G. affinis and G. geiseri, but symmetrical species isolation.     

Paternity Analysis in a Hexapod (Orchesella cincta; Collembola) with Indirect Sperm Transfer

In species where males and females interact during mating, the role of females in sexual selection cannot always be demonstrated unambiguously. Here we present a model system to study female choice for mates. Orchesella cinca is a soil-dwelling hexapod with indirect sperm transfer. Females and males do not interact physically for reproduction. We gave females the choice between spermatophores produced by two different males. Paternity analysis based on microsatellite variation revealed that offspring in one clutch were sired by one male only. Direct observations showed that after a female has taken up a spermatophore, the female's receptivity to further spermatophore uptake seem to end. Our results imply that the female is in full control of paternity.     

Interpopulation variation in female remating is attributable to female and male effects in <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis>

The evolution of female multiple mating is best understood by consideration of male and female reproductive perspectives. Females should usually be selected to remate at their optimum frequencies whereas males should be selected to manipulate female remating to their advantage. Female remating behavior may therefore be changed by variation of male and female traits. In this study, our objective was to separate the effects of female and male strains on female remating for the adzuki bean beetle, Callosobruchus chinensis, for which there is interstrain variation in female remating frequency. We found that interstrain variation in female remating is primarily attributable to female traits, suggesting genetic variation in female receptivity to remating in C. chinensis. Some interstrain variation in female remating propensity was attributable to an interaction between female and male strains, however, with the males of some strains being good at inducing nonreceptivity in females from one high-remating strain whereas others were good at inducing copulation in nonvirgin females from the high-remating strain. There is, therefore, interstrain variation in male ability to deter females from remating and in male ability to mate successfully with nonvirgin females. These results suggest that mating traits have evolved along different trajectories in different strains of C. chinensis.     

Non-lactating versus lactating females: a comparison of sex steroids,sexual coloration,and sexual behavior in Japanese macaques

Female Japanese macaques are seasonal breeders distinguished by their red-colored hindquarters, face, and nipple skin areas. Intensity of coloration seems to be associated with sexual attractiveness, behavior, and fluctuating sex steroids. Our aim was to investigate whether the color intensity of these regions differed between lactating (LA) and non-lactating (NLA) females during sexually inactive (SI) and active (SA) phases. Coloration scores of 19 adult females were classified using color tables. Estrogen and progesterone metabolites were determined in fecal samples. Weekly comparison between both groups revealed significantly increased coloration of the hindquarters area from week 13 (SI) until the end of the observation period, and for the nipple skin throughout the SI and SA periods. Face coloration differed marginally. Hormonally, NLA females showed significantly increased excretion rates of sex steroids at the end of the SI phase and throughout the whole SA period. Logistic regression analyses between elevated fecal steroids and nipple coloration disclosed a significant relationship for NLA females during the SI period. This connection persisted and included hindquarter coloration during the SA period. NLA females showed increased intromission with ejaculation, but no difference was found for intromission without ejaculation. In conclusion, results demonstrate increased endocrine excretion rates for NLA females during the whole observation period, paralleled by an enhanced, fertility-signaling sexual attractiveness.     

Sperm precedence in <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis> estimated using the sterile male technique

P₂, the proportion of offspring sired by the second male to mate, is an indicator of the outcome of postcopulatory sexual selection, which occurs through sperm competition and/or cryptic female choice. We determined the appropriate dose of gamma radiation for sterilization of adult males and, using the sterile male technique, measured P₂ in the adzuki bean beetle, Callosobruchus chinensis. Adult males of C. chinensis were almost completely sterilized when irradiated at 80 Gy. Thus, we obtained sterile males through irradiation at this dose. Neither the probability of female first mating nor the probability of female remating was affected by whether females were paired with normal or sterile males. The P₂ calculated from the hatching success of eggs laid by females that mated both with normal and sterile males did not differ between reciprocal mating sequences, indicating that the sterilization has no effect on sperm fertilizing ability. The P₂ was estimated at 0.25. This study shows that female remating in C. chinensis means the coexistence of sperm from two males and thus the occurrence of postcopulatory sexual selection within the female reproductive tract, resulting in first-male sperm precedence.     

Differences in Mating Propensity Between Immature Female Color Morphs in the Damselfly Ischnura elegans (Insecta: Odonata)

Female-limited color polymorphisms occur in a variety of animal taxa where excessive male sexual harassment may explain the coexistence of multiple female color morphs. In the color polymorphic damselfly Ischnura elegans, mature and immature female color morphs coexist at the mating site where males are in search for suitable mating partners. Here, we study male preference and female mating propensity for the two immature female morphs. As would be expected, compared to mature morphs, both immature female morphs mate much less. Within immature females, one morph consistently mates more frequently compared to the other morph, a pattern that is similar for the ontogenetically corresponding mature female morphs. Preference experiments with the two differently colored immature female morphs, however, did not indicate male mate preference for either morph. Low mating frequencies of immature females at natural sites in combination with relatively high attractiveness of immature models in terms of male preference indicate that female behavior influences female mating success.     

Hormonal regulation of female nuptial coloration in a fish

Physiological color change in camouflage and mating is widespread among fishes, but little is known about the regulation of such temporal changes in nuptial coloration and particularly concerning female coloration. To better understand regulation of nuptial coloration we investigated physiological color change in female two-spotted gobies (Gobiusculus flavescens). Females of this species develop an orange belly that acts as an ornament. The orange color is caused by the color of the gonads combined with the chromathophore based pigmentation and transparency of the skin. Often during courtship and female–female competition, a rapid increase in orange coloration, in combination with lighter sides and back that increases skin and body transparency, gives the belly an intense ‘glowing’ appearance. To understand how this increased orange coloration can be regulated we analysed chromatic and transparency effects of neurohumoral agents on abdominal skin biopsies in vitro. We found prolactin and α-melanocyte stimulating hormone (MSH) to increase orange coloration of the skin. By contrast, melatonin and noradrenaline increased skin transparency, but had a negative effect on orange coloration. However, mixtures of melatonin and MSH, or melatonin and prolactin, increased both orange coloration and transparency. This effect mimics the chromatic ‘glow’ effect that commonly takes place during courtship and intra sexual aggression. Notably, not only epidermal chromatophores but also internal chromatophores lining the peritoneum responded to hormone treatments. There were no chromatic effects of the sex steroids 17β-estradiol, testosterone or 11-ketotestosterone. We hypothesize that similar modulation of nuptial coloration by multiple hormones may be widespread in nature.     

Parturition Signaling by Visual Cues in Female Marmosets (Callithrix jacchus)

New World monkeys have polymorphic color vision, in which all males and some females are dichromats, while most females are trichromats. There is little consensus about which selective pressures fashioned primate color vision, although detection of food, mates and predators has been hypothesized. Behavioral evidence shows that males from different species of Neotropical primates seem to perceive the timing of female conception and gestation, although, no signals fulfilling this function have been identified. Therefore, we used visual models to test the hypothesis that female marmosets show chromatic and/or achromatic cues that may indicate the time of parturition for male and female conspecifics. By recording the reflectance spectra of female marmosets’ (Callithrix jacchus) sexual skin, and running chromatic and achromatic discrimination models, we found that both variables fluctuate during the weeks that precede and succeed parturition, forming “U” and inverted “U” patterns for chromatic and achromatic contrast, respectively. We suggest that variation in skin chroma and luminance might be used by female helpers and dominant females to identify the timing of birth, while achromatic variations may be used as clues by potential fathers to identify pregnancy stage in females and prepare for paternal burdens as well as to detect oestrus in the early post-partum period.     

“Reverse” sexual dichromatism in a Neotropical frog

Sexual dichromatism is widespread among animals, but examples of “reverse” sexual dichromatism, in which females are more brightly colored than males, are extremely rare. We discovered a unique case of reverse sexual dichromatism in the golden rocket frog (Anomaloglossus beebei), a diurnal Neotropical frog. Females are bright “golden” in color, and males are drab tan with brown pigmentation that darkens when they are calling. Here, we document this color variation with calibrated digital photography and further show that there is no evidence for sex‐specific habitat matching; both sexes live in the same well‐lit habitat on green bromeliad leaves. Our results suggest that color variation in this species is an intraspecific signal and provide an important exception to the general expectation that males are more visually conspicuous in species with conventional sex roles.     

Color Vision in <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>: A Behavioral Study

We assessed the color discriminations by golden-headed lion tamarins (Leontopithecus chrysomelas) via a series of tasks involving a behavioral paradigm that maximizes the naturalness of the stimuli. The stimuli were pairs of Munsell color chips used in earlier experiments with human dichromats. We tested 3 male and 3 female monkeys with stimuli of random brightness values in order to assure that discriminations were based on color rather than brightness cues. Results indicate that each male and one female presented random performances for stimuli resembling hue conditions under which tamarins forage: oranges vs. greens. Two females exhibited discriminations consistent with allelic trichromacy. Findings indicate the presence of an M/L cone opsin polymorphism, a condition of most platyrrhines that is characterized by dichromatic and/or trichromatic females and dichromatic males. Interspecific differences in allelic frequency among lion tamarins raises the possibility that habitat fragmentation is affecting heterozygous frequencies, a trend that could impact tamarin foraging efficiency.     

Sexual Isolation Between Drosophila Melanogaster, D. Simulans and D. Mauritiana: Sex and Species Specific Discrimination

The sexual isolation among the related species Drosophila melanogaster, D. simulans and D. mauritiana is asymmetrical. While D. mauritiana males mate well with both D. melanogaster and D. simulans females, females of D. mauritiana discriminate strongly against males of these two species. Similarly, D. simulans males mate with D. melanogaster females but the reciprocal cross is difficult. Interspecific crosses between several populations of the three species were performed to determine if (i) males and females of the same species share a common sexual isolation genetic system, and (ii) males (or females) use the same genetic system to discriminate against females (or males) of the other two species. Results indicate that although differences in male and female isolation depend on the populations tested, the isolation behaviour between a pair of species is highly correlated despite the variations. However, the rank order of the isolation level along the populations was not correlated in both sexes, which suggests that different genes act in male and female sexual isolation. Neither for males nor for females, the isolation behaviour of one species was paralleled in the other two species, which indicates that the genetic systems involved in this trait are species-pair specific. The implications of these results are discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

Nonconceptive Sexual Behavior in Bonobos and Capuchins

Sexual behavior by infecundable females, and by same-sex and adult-immature dyads, occurs in wild and captive bonobos (Pan paniscus). Proposed functions of these behaviors, in social primates generally, include practice, paternity confusion, exchange, and communication as well as appeasement. We used this framework to interpret and to compare observations of sexual behavior in a captive bonobo group and a wild white-faced capuchin (Cebus capucinus) group. In both species, (a) sexual behavior was no more frequent in cycling females than in pregnant or lactating females and (b) same-sex and adult-immature dyads engaged in as much mounting or genitogenital contact as adult heterosexual dyads did. The species differed in that (a) bonobos engaged in sexual behavior 65 times as frequently as capuchins, (b) only bonobos engaged in sexual contact other than ventrodorsal mounting during focal observation, and (c) bonobo sexual contact was concentrated most heavily in socially tense situations in adult female–female dyads, whereas capuchin sexual contact was concentrated most heavily in socially tense situations in adult male–male dyads. These data and published literature indicate that (a) practice sex occurs in both species, (b) paternity confusion may be a current function of C. capucinus nonconceptive sex, (c) exchange sex remains undemonstrated in capuchins, and (d) communication sex is more important to members of the transferring sex—female bonobos and male capuchins—than to members of the philopatric sex.     

Visible skin color distribution plays a role in the perception of age, attractiveness, and health in female faces

Evolutionary psychologists have proposed that preferences for facial characteristics, such as symmetry, averageness, and sexual dimorphism, may reflect adaptations for mate choice because they signal aspects of mate quality. Here, we show that facial skin color distribution significantly influences the perception of age and attractiveness of female faces, independent of facial form and skin surface topography. A set of three-dimensional shape-standardized stimulus faces—varying only in terms of skin color distribution due to variation in biological age and cumulative photodamage—was rated by a panel of naive judges for a variety of perceptual endpoints relating to age, health, and beauty. Shape- and topography-standardized stimulus faces with the homogeneous skin color distribution of young people were perceived as younger and received significantly higher ratings for attractiveness and health than analogous stimuli with the relatively inhomogeneous skin color distribution of more elderly people. Thus, skin color distribution, independent of facial form and skin surface topography, seems to have a major influence on the perception of female facial age and judgments of attractiveness and health as they may signal aspects of underlying physiological condition of an individual relevant for mate choice. We suggest that studies on human physical attractiveness and its perception need to consider the influence of visible skin condition driven by color distribution and differentiate between such effects and beauty-related traits due to facial shape and skin topography.