RoL: COLLABORATIVE RESEARCH: EXTREME ENVIRONMENTS, PHYSIOLOGICAL ADAPTATION, AND THE ORIGIN OF SPECIES

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Extreme environments allow for the investigation of life's capacity and limitations to cope with far-from-average environmental conditions. Springs rich in hydrogen sulfide represent some of the most extreme freshwater environments because hydrogen sulfide halts energy production in animal cells. Nonetheless, some fish have colonized sulfide springs throughout the Americas and have evolved into new species in the process. This project will investigate how the genetic changes that mediate the fish's ability to tolerate hydrogen sulfide impact their ability to successfully interbreed with related fish that live in adjacent freshwater streams. It involves the identification of genetic differences between hydrogen sulfide-tolerant and susceptible populations, particularly in genes associated with pathways affected by hydrogen sulfide toxicity. In addition, it will be tested how hybrids between tolerant and susceptible populations differ from their parents. Specifically, the function of mitochondria and whole organisms will be compared between parents and hybrids in presence or absence of hydrogen sulfide. This project will yield new insights into how adaptation to environmental stress leads to genetic incompatibilities that represent barriers for interbreeding between populations, and thus, into how new species form. This project provides training opportunities in integrative biology for participants at all levels of higher education. It will also contribute to science education and public outreach by training scientists to become effective science communicators and reach non-expert audiences in collaboration with informal education institutions. Natural selection drives adaptive evolution and can cause speciation. However, the potential role of intrinsic genetic incompatibilities during speciation with gene flow remains largely unknown. Investigating speciation with gene flow in the context of physiological adaptation allows closing existing gaps of knowledge. This is possible through integrated analyses of how selection shapes genomic divergence, how recombination of divergent genomes in hybrids affects physiological function, and how these functional consequences affect the speciation process. This project tests a priori predictions about the links between physiological adaptation to toxic hydrogen sulfide and the emergence of reproductive isolation. It will focus on components of a highly conserved metabolic pathway, oxidative phosphorylation (OXPHOS), which plays a central role in adaptation to hydrogen sulfide. Because OXPHOS components are encoded by both the mitochondrial and the nuclear genomes, theory predicts that adaptive modification of OXPHOS should give rise to mitonuclear incompatibilities and contribute to the speciation process. This project investigates the mechanistic links between physiological adaptation and speciation by testing a priori predictions about (1) how OXPHOS adaptation affects genomic divergence between populations living in different environments, (2) the functional consequences of mitonuclear incompatibilities at the biochemical, physiological, and organismal levels, and (3) the relative role of mitonuclear incompatibilities during speciation. The project employs an integrative approach that combines population genomics, assays of enzyme, organelle, and whole organism function, as well as field and laboratory experiments for the quantification of multiple pre- and postzygotic mechanisms of reproductive isolation.This award was co-funded by BIO/Emerging Frontiers, DEB/Evolutionary Processes, and IOS/Integrative Ecological Physiology.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.