The biogeographic and evolutionary processes shaping population divergence in Laupala

Abstract

AbstractSpeciation generates biodiversity and the mechanisms involved are thought to vary across the tree of life and across environments. For example, well‐studied adaptive radiations are thought to be fuelled by divergent ecological selection, but additionally are influenced heavily by biogeographic, genomic and demographic factors. Mechanisms of non‐adaptive radiations, producing ecologically cryptic taxa, have been less well‐studied but should likewise be influenced by these latter factors. Comparing among contexts can help pinpoint universal mechanisms and outcomes, especially if we integrate biogeographic, ecological and evolutionary processes. We investigate population divergence in the swordtail cricket Laupala cerasina, a wide‐spread endemic on Hawai'i Island and one of 38 ecologically cryptic Laupala species. The nine sampled populations show striking population genetic structure at small spatio‐temporal scales. The rapid differentiation among populations and species of Laupala shows that neither a specific geographical context nor ecological opportunity are pre‐requisites for rapid divergence. Spatio‐temporal patterns in population divergence, population size change, and gene flow are aligned with the chronosequence of the four volcanoes on which L. cerasina occurs and reveal the composite effects of geological dynamics and Quaternary climate change on population dynamics. Spatio‐temporal patterns in genetic variation along the genome reveal the interplay of genetic and genomic architecture in shaping population divergence. In early phases of divergence, we find elevated differentiation in genomic regions harbouring mating song loci. In later stages of divergence, we find a signature of linked selection that interacts with recombination rate variation. Comparing our findings with recent work on complementary systems supports the conclusion that mostly universal factors influence the speciation process.