Spring-adapted darters (Percidae: Etheostoma) as a model to understand factors that influence diversification, gene flow, and genetic variation in freshwater fishes

Abstract

Darters (Percidae: Etheostomatinae) represent one of the most successful evolutionary radiations in North America and have become an exceptional model system in the study of freshwater fish diversification. I used a variety of phylogenetic and population genetic methods to determine the utility of coldwater spring inhabiting darters from the Southern Appalachians as a model to understand how demography, ecology, geography, and time interrelate to influence genetic variation, gene flow, and lineage diversification at fine scales within river drainages. Chapters two and three focused on elucidating the colonization history of spring habitats and post-colonization evolution of the spring endemic Etheostoma nuchale; and E. phytophilum;. The analysis suggested that Pleistocene climate fluctuations likely facilitated spring habitat specialization. Both species were highly genetically structured, suggesting reduced dispersal capabilities compared to stream inhabiting sister species. Further, the finding of small long-term effective population sizes suggested that geologic and habitat stability played a key role in their persistence in an extremely isolated setting over evolutionary time scales. Chapter four used the spring endemic E. ditrema; and closely related stream inhabitants to test predictions of peripatric speciation. Phylogeographic reconstructions suggested that Pleistocene climatic fluctuations promoted rapid divergence of marginal spring inhabitants, and species identity has been maintained despite intermittent gene flow with stream relatives. Predictions of peripatric speciation were supported for E. ditrema;, i.e. high levels of population structure, reduced dispersal ability, low levels of genetic variation, and evidence for prolonged bottlenecks compared to stream relatives. This chapter highlighted the importance of both historical and ecological processes in peripatric speciation. Lastly, chapter five used comparative phylogeographic and population genetic methods to investigate the influence of habitat preference on gene flow, dispersal ability, and lineage divergence among two sister species of darters (E. boschungi; and E. tuscumbia;) with differing habitat preferences. The analysis revealed highly incongruent phylogeographic histories, population structures, and patterns of migration between the two species, supporting a previous hypothesis that habitat preference may contribute to lineage diversification in darters, especially by limiting dispersal among large river courses. Both species also showed striking differences in demographic history, suggesting differences in habitat stability during the Pleistocene. These results suggest that the combination of habitat preference and spatiotemporal habitat stability strongly influence gene flow and lineage divergence on fine geographic scales in darters, a finding that has potentially important implications for understanding diversification of the rich North American freshwater fish fauna.