The roles of geographical isolation, secondary contact, and mitonuclear disequilibrium in speciation

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One of the enduring challenges in biology is understanding how new species arise, a challenge that predates Charles Darwin. Although speciation is conceptually simple, involving the evolution of traits that prevent interbreeding of diverged populations, there are key knowledge gaps. For example, why do new sister species often begin as geographically isolated populations and what selective forces cause divergence? What happens when isolated populations come back together, and does this play a role in completing speciation? What genetic changes contribute to the evolution of species? One new idea proposes that proteins encoded by nuclear and mitochondrial genes that perform critical functions (energy production in cells) diverge in among geographically isolated populations, with hybrids between populations having lower fitness because nuclear and mitochondrial encoded proteins do not work well together. Thus a new question for understanding species origins asks if such mitochondrial-nuclear coevolution might cause hybrid disfunction between species. Our proposed NSERC-funded research addresses these questions, focusing on the spring peeper, a small North American treefrog. Previous work reveals a dynamic evolutionary history with 3 nuclear lineages that originated in refugia, and clear zones of secondary contact. We found differences in male advertisement calls and behavior among lineages (calling from the ground or perches). We will use playback experiments to test whether females perceive call differences, and plaster model frogs to assess physiological costs of calling from perches (e.g. evaporative water loss). At 5 known contact zones we will combine genomics, and call analysis and playbacks to evaluate outcomes of contact between previously isolated lineages. We will use functional genomics, physiological, and molecular evolution approaches to test costs of hybridization caused by mismatch between nuclear and mitochondrial encoded proteins. For two congeners of the spring peeper, western and boreal chorus frogs, we will use niche modeling and genomics to test the outcomes of secondary contact, and if interspecific interactions or abiotic factors are more important in shaping species distributions. This research will provide premier training for a minimum of 4 PhD, 3 MSc and >10 BSc students in genomics, quantitative methods, and professional development. This work helps put Canada at the forefront of speciation research, bringing together perspectives from genomics, physiology, biogeography, and spatial ecology. It helps us to understand what factors shape species ranges and how they have shifted in response to past climate change, and can provide inputs into conservation strategies for species at risk; e.g. how best to retain evolutionary potential, and how species' distributions might be affected by climate change. I will also leverage NSERC research to secure other opportunities for conservation studies of Canadian species at risk.