Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles

Abstract

Male–female coevolution has taken different paths among closely related species, but our understanding of the factors that govern its direction is limited. While it is clear that ecological factors, life history, and the economics of reproduction are connected, the divergent links are often obscure. We propose that a complete understanding requires the conceptual integration of metabolic phenotypes. Metabolic rate, a nexus of life history evolution, is constrained by ecological factors and may exert important direct and indirect effects on the evolution of sexual dimorphism. We performed standardized experiments in 12 seed beetle species to gain a rich set of sex-specific measures of metabolic phenotypes, life history traits, and the economics of mating and analyzed our multivariate data using phylogenetic comparative methods. Resting metabolic rate (RMR) showed extensive evolution and evolved more rapidly in males than in females. The evolution of RMR was tightly coupled with a suite of life history traits, describing a pace-of-life syndrome (POLS), with indirect effects on the economics of mating. As predicted, high resource competition was associated with a low RMR and a slow POLS. The cost of mating showed sexually antagonistic coevolution, a hallmark of sexual conflict. The sex-specific costs and benefits of mating were predictably related to ecology, primarily through the evolution of male ejaculate size. Overall, our results support the tenet that resource competition affects metabolic processes that, in turn, have predictable effects on both life history evolution and reproduction, such that ecology shows both direct and indirect effects on male–female coevolution.

Experimental Life History Evolution Results in Sex-specific Evolution of Gene Expression in Seed Beetles

“…The patterns therefore point to a more direct role of the divergent life history regimes. Reduced sexual dimorphism in physiology (metabolic rate) is associated with adaptation to slower pace of life and longer lifespan across seed beetles ( Arnqvist et al 2022 ), echoing the gene expression divergence we observed in a micro-evolutionary scale.…”

“…The temporal window for multiple mating is restricted in E lines (due to a female refractory period of 2 days in this species; Šešlija et al 2009 ). In addition, L females have evolved a higher remating rate ( Šešlija et al 2009 ), likely to extract water and nutrients from male ejaculates to extend their lifespan ( Arnqvist et al 2022 ). Consequently, E males have evolved under relaxed sperm competition compared with the L males, whereas selection on females from mating interactions would also differ between the regimes.…”

Metabolic consequences of sex-reversal in two lizard species: a test of the like genotype and like phenotype hypotheses

“…Resource availability is a limiting factor for many adult lizards in arid and semi-arid environments (Bradshaw, 1997;Congdon, 1989;Kearney & Porter, 2004) occupied by P. vitticeps (Greer, 1989). Resource competition in these systems has been shown to drive selection towards lower metabolic rates when resources are scarce and vice versa when resources are high (Arnqvist et al, 2022;Mueller & Diamond, 2001). The unpredictable resource pulses (high rainfall events/high productivity vs. drought/low productivity) of this region shape demographic processes for other species (Kwok et al, 2016;Letnic & Dickman, 2010;Noy-Meir, 1973).…”

Ecology, the pace‐of‐life, epistatic selection and the maintenance of genetic variation in life‐history genes

“…Suites of correlated behavioural traits are also sometimes incorporated into this framework (Réale et al, 2010). Ecological factors clearly have a central role in POL evolution (Dammhahn et al, 2018) and environmental conditions and suites of LH traits often covary across species in many groups (Stearns, 1983): species experiencing more frequent or severe resource limitation tend to show a slower POL compared to species living in environments where resource competition is less intense (Arnqvist et al, 2022).…”