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Dietary macronutrients regulate life span and aging, yet little is known about their evolutionary effects. Here, we examine the evolutionary response of these traits in decorated crickets (Gryllodes sigillatus) maintained on diets varying in caloric content and protein-to-carbohydrate ratio. After 37 generations, each population was split: half remained on the evolution diet, and half switched to a standardized diet. Crickets lived longer and aged slower when evolving on high-calorie (both sexes) and carbohydrate-biased (females only) diets and had lower baseline mortality on high-calorie (females only) diets. However, on the standardized diet, crickets lived longer when evolving on high-calorie diets (both sexes), aged slower on high-calorie (females only) and carbohydrate-biased (both sexes) diets, and had lower baseline mortality on high-calorie (males only) and protein-biased (both sexes) diets. Life span was longer, and baseline mortality was lower when provided with the evolution vs. the standardized diet, but the aging rate was comparable. Moreover, life span was longer, aging slower (females only), and baseline mortality was lower (males only) compared to our evolved baseline, suggesting varying degrees of dietary adaptation. Collectively, we show dietary components influence the evolution of life span and aging in different ways and highlight the value of combining experimental evolution with nutritional geometry.

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 not only 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.

Abstract

Natural selection (measured via evaporative water loss) and sexual selection (measured via mating success) acting on cuticular hydrocarbons are opposing in male black field crickets (Teleogryllus commodus). This opposing pattern of selection has important implications for how variation is maintained in this important chemical trait.

Despite widespread variation in life span across species, three clear patterns exist: sex differences in life span are ubiquitous, life span is commonly traded against reproduction, and nutrition has a major influence on these traits and how they trade‐off. One process that potentially unites these patterns is intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction. If nutrient intake has sex‐specific effects on life span and reproduction but nutrient choice is genetically linked across the sexes, intralocus sexual conflict will occur and may prevent one or both sexes from feeding to their nutritional optima.

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