Introduction
Darwin posited that sexual selection plays an important role in
improving non-sexual fitness, writing that, “the strongest and most
vigorous males, or those provided with the best weapons, have prevailed
under nature, and have led to the improvement of the natural breed or
species” (Darwin, 1871). The modern version of this idea proposes that
sexually selected traits in males reflect “good genes” (Fisher, 1930;
Zahavi, 1975; Iwasa et al. , 1991; Houle & Kondrashov, 2002),
explaining potentially costly female choice by indirect benefits
received in the form of increased offspring fitness. Theory suggests
expression of sexually-selected traits should evolve to become dependent
on overall condition—which would maintain signal fidelity—leading to
accelerated rates of adaptation (Lorch et al. , 2003) and more
efficient purging of deleterious mutations (Whitlock & Agrawal, 2009).
In line with predictions of positive effects of sexual selection on
population performance, sexual selection has been found to diminish the
likelihood of population extinction (Jarzebowska & Radwan, 2010; Lumleyet al. , 2015). Experimental work in Drosophila has also shown
that the presence of sexual selection accelerates the purging of
deleterious alleles in experimental populations (Radwan, 2004; Holliset al. , 2009; Whitlock & Agrawal, 2009; Grieshop et al. ,
2016). In several experiments, sexual selection facilitated adaptation
to novel environmental challenges, including the evolution of
desiccation resistance in D. melanogaster (Gibson Vega et
al. , 2020), pesticide resistance in Tribolium castaneum (Jacombet al. , 2016), and adaptation to a novel diet inCallosobruchus maculatus (Fricke & Arnqvist, 2007). However, an
arguably larger body of experimental work has found no role for sexual
selection in improving non-sexual fitness. Multiple experimental
evolution studies failed to find population-level net benefits of sexual
selection when examining larval competitive ability, net reproductive
rate, or female fecundity (Promislow et al. , 1998; Holland &
Rice, 1999; Long et al. , 2009 respectively). Moreover, a large
body of work has also failed to demonstrate a role of sexual selection
in adaptation in novel environments (e.g. to higher temperatures
(Holland, 2002) or a novel diet (Rundle et al. , 2006)). There is
also no evidence that overall mutation load from the genome is reduced
under heightened sexual selection (Hollis & Houle, 2011; Arbuthnott &
Rundle, 2012) (although in environments that are spatially complex, this
is not true and the predicted beneficial effects of sexual selection on
mutation load are seen (Singh et al. , 2017)). Thus, taken
together, the literature is equivocal about role of sexual selection in
non-sexual fitness. This leaves an open question about whether the
“good genes” mechanism plays a role in adaptation in general or even
in specific scenarios, like during adaptation to pathogens or parasites,
where this role has been predicted to be most evident but remains
largely untested.
One potential explanation for these mixed results is that the non-sexual
fitness of populations is normally elevated by competition for
mates—that is, sexual selection in the broad sense does have adaptive
value—but these benefits are counterbalanced by the negative effects
of sexual conflict and therefore invisible in many experimental designs.
Sexual conflict arises because of an evolutionary conflict of interests
between the sexes (Parker, 1979; Hosken et al. , 2019) which can
manifest in two ways. The first, interlocus sexual conflict, is
characterized by selection favoring traits that increase male
competitive success even when these traits are accompanied by harm to
females. Interlocus sexual conflict can lead to the evolution of female
resistance and sexually antagonistic coevolution (Holland & Rice,
1999a; Chapman et al. , 2003; Rice et al. , 2006), reducing
mean population fitness (Bonduriansky & Chenoweth, 2009; Long et
al. , 2009, 2012). In Drosophila, interlocus sexual conflict acts
through antagonistic effects on female fecundity and survival (Rice,
1996; Chapman, 2006), especially on the most fecund females (Longet al. , 2009). Intralocus conflict, on the other hand, involves
sexually antagonistic pleiotropic effects of polymorphisms at the same
locus in males and females (Bonduriansky & Chenoweth, 2009; Van Doorn,
2009; Innocenti & Morrow, 2010)) that constrain males and females from
reaching sex-specific optima (Chippindale, 2001; Hollis et al. ,
2014, 2019). Either form of sexual conflict leads to a burden on
populations that might overwhelm any positive effects of sexual
selection for mean population fitness (Bonduriansky & Chenoweth, 2009;
Long et al. , 2009, 2012).
Male-male competition and female choice have been proposed to be
particularly consequential for evolution of pathogen resistance
(Hamilton & Zuk, 1982; Folstad & Karter, 1992; Roberts et al. ,
2004). Pathogens are a major evolutionary driver of the life histories
of organisms (Price, 1980; Schmid-Hempel, 2005) due to their prevalence,
diversity, and because they adapt to the host and represent a moving
target for the immune system. According to the Hamilton-Zuk hypothesis
(1982), sexual ornaments indicate immunity towards prevalent pathogens
or parasites (Hamilton & Zuk, 1982; Martin, 1990). A number of studies
in birds have indeed demonstrated phenotypic correlations between male
parasite or pathogen load and the quality of sexual ornaments (Hamilton
& Zuk, 1982; Martin, 1990; Balenger & Zuk, 2014) or female preference
towards the males (Blount et al. , 2003; Hund et al. ,
2020). Yet, whether this phenotypic correlation should be positive or
negative is not unequivocally predicted by mathematical models; either
may be predicted depending on details of the model assumptions (Getty,
2002). These phenotypic correlations between sexual ornaments and
parasite/pathogen resistance do not necessarily predict whether sexually
attractive fathers will sire resistant offspring; rather, this key
element of the ”good genes” hypothesis is mediated by additive genetic
correlations (Hamilton & Zuk, 1982). One way to test for this genetic
correlation would be to track the evolution of resistance under
controlled laboratory conditions (Kawecki et al. , 2012) where
both the strength of sexual selection and pathogen pressure are
manipulated. If there is an additive genetic correlation between
sexually successful fathers and pathogen-resistant offspring, resistance
should evolve more readily in populations where males also experience
sexual selection.
Selection for improved immunity (including better physiological
responses to immune challenges) in experimental populations has
generally resulted in a robust and rapid response (Armitage &
Siva-Jothy, 2005; Martins et al. , 2013; Joop et al. , 2014;
Ferro et al. , 2019). Two studies that explored the effect of
sexual selection on immunity by experimentally evolving populations with
and without sexual selection have found that males and females diverge
in their investment in innate immunity (measured as phenyloxidase
activity; PO) (Hangartner et al. , 2015; Bagchi et al. ,
2021). In both these studies (one on the flour beetle Tribolium
castaneum and the other on the seed beetle Callosobruchus
maculatus; (Hangartner et al. , 2015; Bagchi et al. , 2021
respectively)), females from polygamous populations had higher levels of
PO than females from monogamous populations, with no effect on males
from either of the two experimental regimes. The higher levels of PO in
females from sexually selected populations did not influence pathogen
clearance in either study, although in one of the studies higher PO
activity was correlated with lower survival in females upon bacterial
infection (Bagchi et al. , 2021). These studies indicate how
sexual selection and sexual conflict can drive sex-specific differences
in male and female immunity. This pattern is not without exceptions; a
study on the yellow dung fly, Scathophaga stercoraria, did not
report sex differences in PO levels in populations evolved with or
without sexual selection (Hosken 2001). Hosken (2001) also found that
monogamous populations had higher PO levels than polygamous populations,
although here also this difference did not translate into differences in
bacterial clearance after infection (Hosken, 2001). The above studies
manipulated the presence or absence of either a pathogen or sexual
selection. In the work reported here, we manipulated both pathogen and
sexual selection in order to test for effects of the presence of each,
as well as any interaction, on the evolution of pathogen resistance.
We carried out a 2-way factorial evolutionary experiment manipulating
sexual selection and exposure to a pathogen. We let replicate
populations of D. melanogaster evolve for 14 generations either
under controlled monogamy or random polygamy (i.e., with or without
sexual selection (Hollis & Houle, 2011)), each generation exposing
males to either an intestinal pathogen (a gram-negative bacteriumPseudomonas entomophila ) or a sham treatment. In our
experimental design, we only exposed males to the pathogen and allowed
the males to interact with females after one day of exposure to the
pathogen (we verified that males had cleared the bacteria from their gut
at this timepoint, and thus did not infect the females). With this
design, we aimed to increase the opportunity for sexual selection to act
via differential mating success of males differentially coping with
infection. We aimed to address several interconnected questions.
First, and most simply, do D. melanogaster populations exposed to
the pathogen as adults evolve resistance, measured as survival after
infection, over a short timescale? Resistance to P. entomophilahas been reported to evolve after only four generations of strong
selection imposed by breeding from flies that survived a prior infection
(Martins et al. , 2013). Second, if only one sex—in our design,
males—experiences the pathogen, would evolved resistance to P.
entomophila be detectable in the other sex? If evolved resistance is
evident in both sexes, this would indicate a shared genetic basis.
Third, would sexual selection lead to the evolution of differences in
pathogen resistance even in the absence of pathogen? This would be
predicted if there were an additive genetic correlation between male
sexual traits and resistance that were expressed irrespective of
pathogen exposure (Joye & Kawecki, 2019). A result supporting this
prediction has been reported in Tribolium (Hangartner et
al. , 2015) and Callosobruchus (Bagchi et al. , 2021);
however, the conclusion was based on quantifying an aspect of immune
response rather than resistance to an actual pathogen. Fourth, does
sexual selection accelerate the evolution of resistance in populations
exposed to the pathogen, and does it do so to a greater degree than
would be expected based on the sum of effects of sexual selection and
pathogen exposure acting alone? This positive interaction between the
effects of pathogen and sexual selection would be expected if heritable
variation in pathogen resistance influenced infected males’ sexual
success.
The rationale of this study relied on the pathogen affecting the sexual
success of males. Therefore, prior to the evolutionary experiment we
tested if infection with P. entomophila affects competitive
paternity share. Mortality in our laboratory population was much lower
than is generally reported (Martins et al. , 2013; Faria et
al. , 2015; Joye & Kawecki, 2019), but uninfected males had greater
competitive paternity success than infected males. If genetic variation
conferring resistance to P. entomophila has a similar positive
effect on male competitive success after exposure to the pathogen, this
scenario should provide an opportunity for female choice to amplify
nonsexual selection and accelerate adaptation to pathogen.