Female ornaments: is red skin color attractive to males and related to condition in rhesus macaques?

Abstract

Sexual selection produces extravagant male traits, such as colorful ornaments, via female mate choice. More rarely, in mating systems in which males allocate mating effort between multiple females, female ornaments may evolve via male mate choice. Females of many anthropoid primates exhibit ornaments that indicate intraindividual cyclical fertility, but which have also been proposed to function as interindividual quality signals. Rhesus macaque females are one such species, exhibiting cyclical facial color variation that indicates ovulatory status, but in which the function of interindividual variation is unknown. We collected digital images of the faces of 32 rhesus macaque adult females. We assessed mating rates, and consortship by males, according to female face coloration. We also assessed whether female coloration was linked to physical (skinfold fat, body mass index) or physiological (fecal glucocorticoid metabolite [fGCM], urinary C-peptide concentrations) condition. We found that redder-faced females were mated more frequently, and consorted for longer periods by top-ranked males. Redder females had higher fGCM concentrations, perhaps related to their increased mating activity and consequent energy mobilization, and blood flow. Prior analyses have shown that female facial redness is a heritable trait, and that redder-faced females have higher annual fecundity, while other evidence suggests that color expression is likely to be a signal rather than a cue. Collectively, the available evidence suggests that female coloration has evolved at least in part via male mate choice. Its evolution as a sexually selected ornament attractive to males is probably attributable to the high female reproductive synchrony found in this species.

Does male mate choice select for female coloration in a promiscuous primate species?

“…However, males appeared to bias their mate choice toward females that had relatively fewer infants during postadulthood, independently of their coloration. This contrasts with previous findings in primates (rhesus macaques: Dubuc et al, 2016;Higham et al, 2011Higham et al, , 2021 and non-primate species (blue tits: Mahr et al, 2012;rock sparrows: Pilastro et al, 2003;Griggio et al, 2009;blue-footed boobies: Torres & Velando, 2005) where female colourful traits positively correlate with reproductive history or success and are attractive to males. It is complicated to interpret this result.…”

“…However, evidence from other primate species suggests that male coloration can vary according to male social characteristics (geladas, Theropithecus gelada: Bergman et al, 2009;snub-nosed monkeys, Rhinopithecus bieti: Grueter et al, 2015; drills, Mandrillus leucophaeus: Marty et al, 2009;rhesus macaques: Petersdorf et al, 2017;mandrills: Setchell & Dixson, 2001) and may influence female mating decisions (rhesus macaques: Dubuc et al, 2016;Waitt et al, 2003). Nonetheless, it should be noted that promiscuous mating, female reproductive synchrony, and strong intrasexual competition have been recently suggested to explain the evolution of female (and male) colourful and attractive ornaments in another primate species (rhesus macaques: Higham et al, 2021). Clearly, further studies are needed to better understand the role of socio-sexual and environmental pressures on the evolution and signalling function of both female-specific and mutual ornamentations across taxa.…”

“…Males may thus express no preference for such traits (three spined sticklebacks, Gasterosteus aculeatus: Wright et al, 2015) or preference may be merely explained by sensory exploitation rather than sexual selection (sockeye salmons, Oncorhynchus nerka: Foote et al, 2004). Alternatively, males can express preferences toward non-sex-specific colourful ornaments that reflect female reproductive state (rhesus macaque, Macaca mulatta: Dubuc et al, 2009;Higham et al, 2010Higham et al, , 2011Higham et al, , 2021; agamid lizards, Ctenophorus ornatus: LeBas & Marshall, 2000) or reproductive success (blue tits, Cyanistes caeruleus: Doutrelant et al, 2008Doutrelant et al, , 2012Mahr et al, 2012;rhesus macaques: Dubuc, Winters, et al, 2014;Higham et al, 2021; rock sparrows, Petroni petronia: Pilastro et al, 2003;Griggio et al, 2009Griggio et al, , 2005; brown boobies, Sula leucogaster: Montoya et al, 2018;blue-footed boobies, Sula nebouxii: Torres & Velando, 2005). Therefore, in these species, female colourful ornaments may be key components of mating strategies and reproductive success of both males and females.…”

Variation and heritability of retinal cone ratios in a free‐ranging population of rhesus macaques

“…2014; Higham et al. 2021), and this is likely true of other catarrhine monkeys (Setchell et al. 2006; Kamilar et al.…”

Oxytocin and testosterone administration amplify viewing preferences for sexual images in male rhesus macaques

“…In females, the coloration of these ‘sexual skins’ intensifies during the mating season due to increased vascular blood flow under the skin surface [ 37 , 41 ], and they tend to be the darkest around ovulation [ 42 , 43 ], thus broadcasting reproductive status to conspecifics. Even though the colour expressed in face and AGR are significantly correlated (for example, in mandrills [ 44 ], drills [ 45 ] and macaques [ 46 ]), it is unclear which area contains more accurate information about the reproductive cycle [ 42 ], and which region attracts more attention from conspecifics [ 39 , 47 ]. In male macaques, sexual skins also darken during the mating season [ 11 , 13 ], but it is unclear precisely what these sexual skins signal.…”