Beauty or function? The opposing effects of natural and sexual selection on cuticular hydrocarbons in male black field crickets

Although many theoretical models of male sexual trait evolution assume
that sexual selection is countered by natural selection, direct empirical
tests of this assumption are relatively uncommon. Cuticular hydrocarbons
(CHCs) are known to play an important role in restricting evaporative
water loss but also in sexual signalling in most terrestrial arthropods.
Insects adjusting their CHC layer for optimal desiccation resistance is
often thought to come at the expense of successful sexual attraction
suggesting that natural and sexual selection are in opposition for this
trait. In this study, we sampled the CHCs of male black field crickets
(Teleogryllus commodus) using solid-phase microextraction and then either
measured their evaporative water loss or mating success. We then used
multivariate selection analysis to quantify the strength and form of
natural and sexual selection targeting male CHCs. Both natural and sexual
selection imposed significant linear and stabilizing selection on male
CHCs, although for very different combinations. Natural selection largely
favoured an increase in the total abundance of CHCs, especially those with
a longer chain length. In contrast, mating success peaked at a lower total
abundance of CHCs and declined as CHC abundance increased. However, mating
success did improve with an increase in a number of specific CHC
components that also increased evaporative water loss. Importantly, this
resulted in the combination of male CHCs favoured by natural selection and
sexual selection being strongly opposing. Our findings suggest that the
balance between natural and sexual selection is likely to play an
important role in the evolution of male CHCs in T. commodus and may help
explain why CHCs are so divergent across populations and species.