Untangling links between mating, plasticity, and invasiveness using widow spiders

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I study how populations are shaped by variable ecological and demographic conditions via the fitness effects of reproductive traits. Given rapid environmental change and rampant biological invasions, understanding determinants of reproductive success and population persistence is urgent. My long-term goal is to understand how reproductive behaviours are tied to the evolution of local adaptation vs phenotypic plasticity (individual variation in phenotypic expression of different genotypes) in variable environments. A growing body of work suggests the importance of plasticity in population persistence and invasiveness. Nevertheless, recent reviews highlight fundamental questions about plasticity that remain unanswered, including whether plasticity itself is adaptive and whether it facilitates or constrains local adaptation. In this proposal, I test hypotheses about how fluctuations in population density and sex ratio can lead to divergent sexual selection and the evolution of socially cued plasticity. This involves juveniles detecting cues that predict the social challenges they will face as adults, and adjusting their development accordingly. The phenotypes or behaviours that develop increase individual success under fluctuating conditions, and at the population level, can increase invasive potential in novel habitats. I will test predictions of our current framework for understanding the evolution of plasticity using a detailed knowledge of ecology and behaviour in Latrodectus spiders (widow spider species), and a developing understanding of the genus Steatoda (false widows). Both genera include species that are successful global invaders, as well as similar congeners that are not invasive despite repeated introductions. Latrodectus species exhibit some of the most extreme mating documented to date, including sexual cannibalism, sperm plugs, high mortality during mate search, and mating with immature females. All of these traits may lead to intense sexual selection, acutely tuned to population density and sex ratio. I propose integrated field and laboratory studies, engaging trainees at all levels, that focus on three objectives. First, identifying determinants of reproductive success in variable environments as a function of density and sex ratio. Second, determining how adult trait expression is linked to fitness, and the social cues that predict that relationship. Third, identifying the gene expression changes that underlie plasticity. Over 20 years of study of Latrodectus spiders with trainees and collaborators has yielded a thorough understanding of how reproductive fitness depends on different aspects of their biology, ecology, and shifting sexual selection. Combined with emerging molecular tools for spiders, this knowledge will ensure that the work proposed here will advance our understanding of plasticity, resilience, and invasiveness under environmental change, and cement Latrodectus as a `model clade' for the study of plasticity.