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.