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.

To estimate sexual selection, we estimated the mating success of 300 males using no-choice trials. This involved placing a randomly selected virgin with each male and recording whether he achieved a mating in a 20-minute period. To estimate natural selection, we measured the evaporative water loss of 300 males using a custom-built device that passed dry purified air over male crickets for a 2-hour period. The difference in the weight of the cricket before and after being placed in this apparatus was taken as the evaporative water loss. Prior to assessing mating success (for sexual selection) and evaporative water loss (for natural selection), we sampled the cuticular hydrocarbon (CHC) profile of each male using solid phase microextraction (SPME) fibers and ran these samples using gas-chromatography mass spectrometry (GCMS) to measure the CHCs using established protocols. Sexual and natural selection were estimated using the standard procedures of multivariate selection analysis.

Excel is required to open the data files.Funding provided by: Royal SocietyCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000288Award Number: UF0762844Funding provided by: Natural Environment Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000270Award Number: NE/G00949X/1Funding provided by: Australian Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000923Award Number: DP180101708Funding provided by: National Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000001Award Number: CMII 1634878