Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations

Abstract

Despite limitations on offspring production, almost all multicellular species use sex to reproduce. Sex gives rise to sexual selection, a widespread force operating through competition and choice within reproduction, however, it remains unclear whether sexual selection is beneficial for total lineage fitness, or if it acts as a constraint. Sexual selection could be a positive force because of selection on improved individual condition and purging of mutation load, summing into lineages with superior fitness. On the other hand, sexual selection could negate potential net fitness through the actions of sexual conflict, or because of tensions between investment in sexually selected and naturally selected traits. Here, we explore these ideas using a multigenerational invasion challenge to measure consequences of sexual selection for the overall net fitness of a lineage. After applying experimental evolution under strong versus weak regimes of sexual selection for 77 generations with the flour beetle Tribolium castaneum, we measured the overall ability of introductions from either regime to invade into conspecific competitor populations across eight generations. Results showed that populations from stronger sexual selection backgrounds had superior net fitness, invading more rapidly and completely than counterparts from weak sexual selection backgrounds. Despite comprising only 10% of each population at the start of the invasion experiment, colonizations from strong sexual selection histories eventually achieved near‐total introgression, almost completely eliminating the original competitor genotype. Population genetic simulations using the design and parameters of our experiment indicate that this invasion superiority could be explained if strong sexual selection had improved both juvenile and adult fitness, in both sexes. Using a combination of empirical and modeling approaches, our findings therefore reveal positive and wide‐reaching impacts of sexual selection for net population fitness when facing the broad challenge of invading competitor populations across multiple generations.

Mating patterns influence vulnerability to the extinction vortex

“…(1) = 0.78, p = .67, polyandry χ 2 (1) = 5.19, p = .07), indicating similar responses to the three different stresses conspecific competitors (Godwin et al, 2018). Here, we now demonstrate applied benefits of sexual selection for population and lineage fitness by revealing that an evolutionary history of enforced monogamy with low sexual selection weakens the ability of populations and lineages to cope with multiple interacting anthropogenic challenges through an extinction vortex.…”

“…Monogamous pairs were maintained and mated in containers containing 2 g flour medium, and polyandrous groups were maintained and mated in containers with 6 g flour medium, therefore allocating 1 g flour medium per adult throughout. After reproduction, adults were removed and eggs/larvae pooled from the multiple pairs or groups within each line, with the flour medium increased and equalized between regimes to 100 g and left to develop under standardized conditions until pupae were ready for the next generation (Godwin et al, 2018;Lumley et al, 2015).…”

“…(b) a polyandry regime, in which female promiscuity was generated by allowing five males to compete for reproduction with a single female (see Demont et al, 2014;Lumley et al, 2015). All individuals originated from the same ancestral stock population, and all other variables (including effective population size and genetic diversity) had been equalized through experimental evolution (see full details in Godwin et al, 2017Godwin et al, , 2018Lumley et al, 2015), allowing us to test how mating pattern and sexual selection influence a population's ability to cope with the extinction vortex.…”

Tribolium beetles as a model system in evolution and ecology

“…Prokop et al 2019 ). A population history (up to ten years) of experimentally applied, strong sexual selection has also been shown to improve the competitive ability of males and their sperm, and drive sperm morphology evolution (Michalczyk et al 2011 ; Demont et al 2014 ; Godwin et al 2017 ), increase conspecific population invasion success (Godwin et al 2018 ), enable population resilience to the extinction vortex (Godwin et al 2020 ), and increase the rate of pesticide resistance evolution (Jacomb et al 2016 ).…”

Polyandry provides reproductive and genetic benefits in colonising populations

“…Experimental studies in this species have shown that founder effects have pronounced costs as a result of genetic and demographic effects and that colonising populations are able to rapidly adapt to novel environments (Szucs, Melbourne, Tuff, & Hufbauer, 2014; Szucs, Melbourne, Tuff, Weiss‐Lehman, & Hufbauer, 2017). Further, this species is promiscuous, and experimental evolution studies have shown that a history of strong sexual selection results in decreased risk of extinction under inbreeding and improved invasion into competitor populations (Godwin et al., 2018; Lumley et al., 2015). Moreover, matings and fertility often appear to fail in this species (Tyler & Tregenza, 2013), and there is some evidence to suggest that these costs are reduced when females mate multiply (Pai, Bennett, & Yan, 2005).…”