Introduction
Male reproduction is a zero-sum game that can lead to intense competition (Weir et al., 2011). Because actual fighting is energetically costly and exposes both the winner and loser to injury and infection, rival males can benefit from displaying their strength or condition using signals that allow for competition without costly engagement in fighting (Bradbury & Vehrencamp, 2011; Maynard Smith & Parker, 1976). The conspicuous male traits used for rival assessment (sexually selected signals) allow for conflict resolution at the lowest cost to both males (Maynard Smith, 1982; Maynard Smith & Harper, 2003, 1995), and are often condition-dependent, such that they reliably indicate some aspect of “quality” that predicts their ability to win a physical fight (i.e., body size, body condition, current health status) (Fisher, 1915; Penn & Számadó, 2020; Trivers, 1972; Zahavi, 1977). Because the expression of the signal is limited by a male’s condition, these signals tend to be honest indicators of ability because only high-quality males can produce the strongest signals (Weaver et al., 2017).
While the functional consequences of signals can be observed noninvasively and are thus relatively well-studied, the mechanisms underlying these traits are much less well-understood. For example, although observational data demonstrate that higher ranking male drills (Mandrillus leucophaeus ) exhibit redder lip and groin coloration than lower ranking males (Marty et al., 2009), identifying the causal mechanism of this difference would require invasive methods such as surgical implantation of slow-release hormone devices, social manipulation, or genetic manipulation, which are often not possible or ethical to conduct in wild populations (Emlen et al., 2012; Hau et al., 2000; Karubian et al., 2011). However, capture-and-release programs in wild populations allow tissue sample collection for genomic and transcriptomic analyses (Tung et al., 2010), providing a minimally invasive technique to investigate the molecular correlates of signal mechanisms without experimental manipulation.
Here we investigated the mechanisms underlying a visual signal that may mediate male competition in a wild primate: the brilliant red chest patch in male geladas (Theropithecus gelada ), a cercopithecine primate endemic to the highlands of Ethiopia. Geladas have a multi-tiered social system in which multiple ‘reproductive units’ (one dominant adult male, one or more subordinate adult males, up to a dozen adult females, and related offspring) associate to forage, rest, and move. The dominant “leader” male of units have the majority of the mating opportunities and display the reddest chests as compared to the subordinate “follower” males (with many fewer reproductive opportunities) and “bachelor” males living in all-male groups (with no reproductive opportunities) (Bergman et al., 2009; Bergman & Beehner, 2008). Because geladas live in large, fluid societies where males frequently congregate and forage with other males that they do not recognize individually (Bergman, 2010), the chest patch is hypothesized to be a sexually selected signal that mediates male rival assessment and allows males to “size up” others prior to engaging in conflict (Benítez, 2016). Bachelor males, which tend to be young adult males awaiting their chance to overthrow and replace leader males (Pappano & Beehner, 2014), are particularly attentive to leader male chest color. For example, across a one-year study, leaders with redder chests (after a vigorous ritualized “vocal display” accompanied by running, throwing rocks, climbing trees, or shaking branches) were less likely to be overthrown by bachelors than their less-red counterparts (Benítez, 2016).
Previous research conducted on the same population has shown that chest redness in geladas is mediated by increased blood flow with a concomitant increase in surface temperature. Specifically, redder chests are associated with (1) increased physical activity (Bergman et al., 2009; DeLacey et al., 2022) and (2) higher chest skin surface temperature, whether measured using internal body heat or following the application of an external heat pack (DeLacey et al., 2022). The relationship with physical activity could be similar to skin flushing in humans during exercise, when skin blood flow increases to dissipate heat generated by muscle contractions (Kenney & Johnson, 1992).
Sexually selected signals in males are often mediated by testosterone, a steroid hormone involved in regulation of reproductive function in male vertebrates (Ketterson & Nolan, 1999; Plant & Zeleznik, 2014) that is associated with reproductive benefits (Enstrom et al., 1997) and physiological costs (Muehlenbein et al., 2006; Muehlenbein & Bribiescas, 2005). High doses of circulating testosterone are known to dilate vascular networks and increase blood flow, providing an avenue for testosterone to work alongside a blood flow mechanism to influence chest redness in geladas (Molinari et al., 2002; Webb et al., 1999). Testosterone can alter gene transcription by: (1) binding to the androgen receptor (AR), (2) aromatizing to estradiol and then binding to estrogen receptor \(\alpha\) (ER\(\alpha\)) or \(\beta\)(ER\(\beta\)), or (3) converting to 5\(\alpha\)-reductase which binds to AR but cannot convert to estradiol (Hau & Wingfield, 2011). Local conversion of testosterone to estradiol is a particularly strong candidate for chest redness regulation based on the results of a similar study; in the closely related male rhesus macaque (Macaca mulatta ), increases in testosterone increased both redness and blood flow in sex skin areas. Moreover, administration of an aromatase inhibitor (which prevents the conversion of testosterone to estradiol) decreased skin redness (Rhodes et al., 1997).
Therefore, to better understand molecular correlates of the chest patch signal mechanism, we collected chest skin biopsies from male and female geladas from a wild population in Ethiopia during non-lethal, immobilizations (hereafter “capture-and-release”) to explore differences in gene expression local to the chest patch. Digital photographs complement this dataset to assess variability in male and female chest redness both in natural conditions and while under anesthesia. We tested the hypothesis that male chest redness is a condition-dependent signal used during rival assessment. We predicted that, when compared to females, males would have: (1) redder chests and a larger within-individual range in chest redness under natural conditions and while under anesthesia, (2) increased expression of genes associated with vascularization, and (3) increased expression of genes associated with androgen and estrogen regulation.