Discussion
We sampled chest skin biopsies from wild geladas to directly measure putative mechanisms underlying a uniquely evolved sexual signal. We found that male and female geladas showed a substantial overlap in chest redness under natural and unmanipulated conditions, but males exhibited a wider within-individual range in baseline redness under natural conditions (Figs. 1-2) . Further, subadults displayed an intermediate gene-expression pattern from adult males and adult females (Fig. 3 ). We also found sex differences in gene expression, where higher expression in males was associated with angiogenesis, blood pressure, and blood vessel maintenance, suggesting that blood flow and vascularization may underlie sex differences in this sexually-selected signal (Fig. 4 ). Contrary to our predictions, genes encoding proteins that interact with androgen or estrogen were not more highly expressed in males. Together, these results suggest that males may have more variable chest redness due to increased blood flow and blood vessel branching in the chest skin.
Chest photograph measurements revealed an overlap in redness between the sexes at baseline in both natural and anesthetized conditions, but males overall exhibited a wider within-individual range in redness. Selection on an ornamentation trait in one sex can create a correlated response in the opposite sex within a species (e.g., male and female coloration are highly correlated in passerines), suggesting that changes in one sex can be constrained by changes in the other sex (Dale et al., 2015; Poissant et al., 2010; Potti & Canal, 2011). In geladas, this overlap in chest redness between the sexes could simply be the result of a positive genetic correlation. Alternatively, as male and female color traits function differently, female chest redness in geladas could have continued to evolve under a different selective pressure (Dale et al., 2015; Tobias et al., 2012), and the overlap in redness could be caused by each sex using the chest patch to communicate different signals. In males, chest redness varies among males by status (Bergman et al., 2009) and within males by activity level (DeLacey et al., 2022), suggesting the chest patch aids in male-male competition. Females have instead co-opted chest redness to communicate reproductive status through hormonal and blood signaling as they have the reddest chests late in gestation when estrogen levels and blood volume are the highest (Hytten, 1985; Roberts et al., 2017). In addition to chest color variation, gelada females exhibit sexual swellings consisting of cutaneous vesicles surrounding the chest region where vesicle turgidity varies across the ovarian cycle, suggesting sexual swellings work in tandem with chest redness to signal a different aspect of reproductive state (Roberts et al., 2017).
The sex difference in gelada chest skin gene expression aligns with findings in humans where a wide variety of tissues exhibit small effects of sex on gene expression (Lopes-Ramos et al., 2020; Oliva et al., 2020). However, small expression changes have been shown to have large phenotypic effects, particularly in the manifestation of disease (Khramtsova et al., 2019). Within primates, sex-biased gene expression has also been detected in rank-related genes, immune regulation, and aging in wild baboons through blood sampling (Anderson et al., 2021; Lea et al., 2018). The magnitude of sex-biased gene expression has been shown to increase across development with the greatest differences in adult tissue (Mank et al., 2010; Perry et al., 2014), and differences are particularly exaggerated in sexually dimorphic tissues such as elaborated weaponry (Zinna et al., 2018). Subadult geladas showed an intermediate pattern of gene expression between that of adult males and females suggesting that gene expression differences increase at sexual maturity when sexually selected signals develop for mate acquisition. Further, an analysis of an avian clade that found the degree of sexual selection predicts the proportion of male-biased gene expression (Harrison et al., 2015). This finding is consistent with gelada chest skin, as we found more genes that were more highly expressed in males compared to genes that were more highly expressed in females in this species with a high male reproductive skew.
​​Male geladas expressed genes associated with angiogenesis, blood pressure regulation, and blood vessel maintenance more highly than females. The mechanism of increased blood vessel branching in the chest skin may indicate chest redness is a condition-dependent signal where the differential costs of signaling based on current body condition inhibit low-quality males from investing in the signal (Grafen, 1990; Penn & Számadó, 2020). We propose energy balance and heat loss as possible costs associated with producing a red chest. Male geladas may develop more extensive blood vessel branching in the skin compared to females through engaging in vocal displays. Post-display chest redness increases with display rate per hour in gelada males (Benítez, 2016) which suggests that after frequent activity has built up vascular networks, an instance of increased blood flow will prompt a larger increase in chest redness. Among males, leaders spend less time resting, more time engaging in low-intensity aggression, and produce more calls per vocal display bout compared to bachelors (Benítez et al., 2016; Perlman, 2021). The physical effort required to engage in aggression and vocal displays may contribute to ensuring only high-quality males in good body condition have red chests (if it is difficult to break the link between exertion and vascularization). Further, redder chests have higher surface skin temperatures which indicates the increased blood flow to this area may also result in heat loss in the cold, high-altitude environment of the Simien Mountains (DeLacey et al., 2022). These potential constraints could provide an avenue for chest redness to communicate current body condition to potential rivals.
Contrary to our predictions, males did not have increased expression of genes associated with androgen and estrogen regulation in the chest skin. Although this result could simply indicate that androgen and estrogen regulation are not important to sex differences in chest redness, it could also (1) indicate both males and females use the same androgen and estrogen regulation pathways in the chest skin or (2) be a product of sequencing skin biopsies in particular as sex-biased genes have tissue-specific expression profiles (Lopes-Ramos et al., 2020; Yang et al., 2006). Perhaps we would detect more sex differences in expression in brain regions involved in the regulation of hormone secretion rather than the target tissue (Becker et al., 2007). Additionally, we measured the expression of genes that interact with estrogen and androgen receptors, but circulating hormones such as testosterone or changes in androgen receptor density may play a larger role in regulating redness in primates (Dixson, 1983; Rhodes et al., 1997; Setchell & Dixson, 2001). As yet, no relationship has been identified between testosterone and chest redness in adult male geladas (DeLacey and Beehner, unpublished data). This may be because this putative signal is not testosterone dependent, or because we are only able to measure fecal androgen metabolite levels (capturing an averaged level of the hormone over the past day) rather than actual circulating testosterone levels. Further, we may not detect a relationship between testosterone and chest redness because estrogens directly regulate chest redness and testosterone only indirectly influences redness through aromatization to estrogens.