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.