Heat stress reveals a fertility debt owing to postcopulatory sexual selection

Climates are changing rapidly, demanding equally rapid adaptation of
natural populations. Whether sexual selection can aid such adaptation is
under debate; while sexual selection should promote adaptation when
individuals with high mating success are also best adapted to their local
surroundings, the expression of sexually selected traits can incur costs.
Here we asked what the demographic consequences of such costs may be once
climates change to become harsher and the strength of natural selection
increases. We investigated how an evolutionary history of strong
postcopulatory sexual selection (sperm competition) affects male fertility
under acute adult heat stress. Harnessing the empirical potential of
long-term experimental evolution in the seed beetle Callosobruchus
maculatus, we assessed the thermal sensitivity of fertility (TSF) in
replicated lines maintained for 68 generations under three alternative
mating regimes manipulating the opportunity for sexual and natural
selection. We find that males evolving under strong sexual selection
suffer from increased TSF, and that male success in sperm competition (P2:
sperm offense) is genetically correlated to increased TSF. Interestingly,
females from the regime under strong sexual selection, who experienced
relaxed selection on their own reproductive effort, had high fertility in
benign settings but suffered increased TSF, like their brothers. This
implies that female fertility and TSF evolved through genetic correlation
with reproductive traits sexually selected in males. Paternal but not
maternal heat stress reduced offspring fertility with no evidence for
adaptive transgenerational plasticity among heat-exposed offspring,
indicating that the observed effects may compound over generations. Our
results suggest that trade-offs between fertility and traits increasing
success in postcopulatory sexual selection can be revealed in harsh
environments. This can put polyandrous species under increased risk during
extreme heat waves expected under future climate change.