Discussion
In our study, we aimed to address the interplay of sexual selection and
pathogen presence on the evolution of resistance to a pathogen, P.
entomophila . We found a signature of pathogen resistance in populations
evolved under pathogen pressure for fourteen generations when compared
to populations evolved without it. Surprisingly, despite only infecting
males over the course of experimental evolution, resistance to pathogen
was more prominent in females. We did not find any evidence that sexual
selection can promote the evolution of resistance to the pathogen,
contrary to the predictions of theory (Hamilton & Zuk, 1982; Westneat
& Birkhead, 1998). We expected that the presence of sexual selection
and pathogen pressure would act synergistically, resulting in a greater
response to selection and therefore improved survival post-infection. We
instead found an antagonistic interaction between the two in males,
which could have possibly impeded the evolution of pathogen resistance.
Evolution of increased resistance of D. melanogaster to enteric
infection and systemic infection has been seen in studies that have
experimentally evolved fly populations with P. entomophila(Martins et al. , 2013; Gupta et al. , 2016). The study by
Martins et al. (2013) imposed very strong selection on both
sexes, with pathogen-induced mortality up to 77% in the initial
generations. In our experiment, pathogen selection was only applied on
males and was associated with much lower mortality (5-25% depending on
the generation). This lower virulence likely resulted from a difference
in the bacterial genotype and/or the initial Drosophila gene pool; the
IV population is generally robust and harbors high levels of genetic
variation. It is likely that the overall strength of selection for
resistance was therefore considerably lower in our experiment, but yet
still sufficient to generate a detectable response. A stronger response
to selection might have been obtained with a more virulent pathogen, or
if both males and females had been infected each generation. Infecting
females introduces a difficulty, however, in that reductions in female
mating rate and fecundity make maintenance of experimental populations
more challenging, and any reductions in female choosiness due to
infection would be expected to diminish the importance of sexual
selection.
The fact that females from populations under pathogen pressure evolved
higher resistance despite not experiencing direct selection supports a
shared genetic basis for immunity between the sexes. Indeed, in line
with this idea (Collet et al. , 2016; Connallon & Hall, 2016),
adaptation to desiccation resistance in experimentally evolved
populations of D. melanogaster was observed both in males and
females even when selection was imposed only on males (Gibson Vegaet al. , 2020). Adaptation in our experiment may also be more
evident in female post-infection survival simply because females show
generally lower survival upon infection relative to males, which would
make any evolved differences in survival easier to detect in females
than males. Moreover, it is also plausible that alleles contributing to
immunity that were favored in males under pathogen pressure had a larger
effect size on resistance in females, making female resistance towards
pathogen more detectable in this sex. We can exclude the possibility
that selection did in fact act directly on females, for example by
sexual or social transmission of the pathogen from males to females,
because the pathogen was cleared by males by the time they encountered
females.
In our study, we do not see any evidence that sexual selection aids the
evolution of resistance to pathogen. Previous studies have attributed
the lack of adaptation to novel environments to the negative effects of
sexual conflict (Holland & Rice, 1999b; Rundle et al. , 2006).
However, if sexual conflict negatively affected adaptation in our
populations we would have expected to find that populations exposed to
the pathogen each generation but not experiencing sexual selection (-SS
+P) would show a stronger signal of adaptation to pathogen than those
exposed to pathogen and experiencing sexual selection (+SS +P). While
our results on male survival after infection align with this idea, there
is no signal of a cost to sexual selection in female survival after
infection, leaving it difficult to attribute any importance to sexual
conflict in our experiment.
In conclusion, our study found that populations of D.
melanogaster evolved resistance to the insect pathogen P.
entomophila , but this was either not facilitated (in females) or
hindered (in males) by sexual selection. We expect that the low
mortality in our study compared to previous work on this pathogen (Guptaet al. , 2013, 2016; Martins et al. , 2013; Joye & Kawecki,
2019), in which the majority of infected individuals die, provided a
level of biological realism. The pathogen was still virulent enough to
induce downstream effects on male sexual success, suggesting that
genetic variation conferring resistance to pathogen would provide a
large target for sexual selection. In addition, because most males
survived infection during the course of experimental evolution, this
provided an opportunity for sexual selection to reinforce non-sexual
selection by magnifying more subtle differences in pathogen resistance
(e.g. differences in male condition or vigor that might emerge after
weathering the infection). Despite a scenario that seems favorable for
the detection of putative benefits of sexual selection—a relatively
mild pathogen that might persist in natural host populations, that still
yet influences mating success, in a host that harbors genetic variation
for resistance—we found no such benefits.