An evolutionary innovation for mating facilitates ecological niche expansion and buffers species against climate change

Abstract

One of the drivers of life’s diversification has been the emergence of “evolutionary innovations”: The evolution of traits that grant access to underused ecological niches. Since ecological interactions can occur separately from mating, mating-related traits have not traditionally been considered factors in niche evolution. However, in order to persist in their environment, animals need to successfully mate just as much as they need to survive. Innovations that facilitate mating activity may therefore be an overlooked determinant of species’ ecological limits. Here, we show that species’ historical niches and responses to contemporary climate change are shaped by an innovation involved in mating—a waxy, ultra-violet-reflective pruinescence produced by male dragonflies. Physiological experiments in two species demonstrate that pruinescence reduces heating and water loss. Phylogenetic analyses show that pruinescence is gained after taxa begin adopting a thermohydrically stressful mating behavior. Further comparative analyses reveal that pruinose species are more likely to breed in exposed, open-canopy microhabitats. Biogeographic analyses uncover that pruinose species occupy warmer and drier regions in North America. Citizen-science observations of Pachydiplax longipennis suggest that the extent of pruinescence can be optimized to match the local conditions. Finally, temporal analyses indicate that pruinose species have been buffered against contemporary climate change. Overall, these historical and contemporary patterns show that successful mating can shape species’ niche limits in the same way as growth and survival.