Isolation and Gene Flow in a Speciation Continuum in Newts

Abstract

Because reproductive isolation often evolves gradually, differentiating lineages may retain the potential for genetic exchange for prolonged periods, providing an opportunity to quantify and understand the fundamental role of gene flow during speciation. Here we delimit taxa, reconstruct the phylogeny and infer gene flow in newts of the Lissotriton vulgaris species complex based on 74 nuclear markers sampled from 127 localities. We demonstrate that distinct lineages along the speciation continuum in newts exchange nontrivial amounts of genes, affecting their evolutionary trajectories. By integrating a wide array of methods, we delimit nine taxa and show that two principle factors have driven their genetic differentiation: time since the last common ancestor determining levels of shared ancestral polymorphism, and shifts in geographic distributions determining the extent of secondary contact. Post-divergence gene flow, indicative of evolutionary non-independence, has been most extensive between sister and non-sister taxa in Central Europe, while four southern European lineages have acquired the population genetic hallmarks of independent species (L. graecus, L. kosswigi, L. lantzi, L. schmidtleri). We obtained strong statistical support for widespread mtDNA introgression, previously suggested by discordance between mtDNA phylogeny and morphology. Our study suggests that long-term evolution in structured populations that may periodically exchange genes may be common: although some of these populations may become extinct or fuse, others will acquire complete reproductive isolation and will carry signatures of this complex history in their genomes.