EVOLUTIONARY GENOMICS OF ATLANTIC MOLLIES ADAPTED TO HYDROGEN-SULFIDE-RICH ENVIRONMENTS

Anthony Paul Brown

Populations adapted to extreme environments, which are typically characterized by harsh physiochemical stressors and reduced species richness, offer unique opportunities to address important questions in evolutionary biology. Using populations of the Atlantic molly (Poecilia mexicana) that independently colonized multiple hydrogen-sulfide-rich springs in Mexico, we addressed three major questions: (1) How does living in a small environment affect the genetic diversity of a population? (2) Is there concordance between nucleotide divergence and gene expression change after colonization of a novel environment? (3) Does convergent genetic evolution underlie convergent phenotypic evolution in extremophile populations? For the first question, we analyzed genetic data from three populations that have resided in sulfidic springs for the longest amount of time. We found that, in contrast to other species affected by human-induced habitat fragmentation, these populations displayed no evidence of inbreeding and had higher levels of genetic variation than expected. For the second question, we analyzed RNA-sequencing data from four populations, two sulfidic and two non-sulfidic, to address whether there was a correlation between nucleotide changes and expression differences upon colonization of a novel environment. Contrary to results from comparisons between distantly related species, we found more genes than expected that were both under positive selection and differentially expressed, indicating that these two processes may be working in concert. For the third question, we used whole genome data from ten individuals to investigate patterns of local ancestry and structural variation throughout the genome. We identified some degree of genetic convergence underlying the convergent phenotypic evolution observed in these populations. We found that ~1.2% of the genome was more similar between individuals from independently derived sulfidic populations than non-sulfidic individuals, but there were few shared structural variants among sulfidic individuals. There were several candidate genes related to survival in sulfide-rich environments that were in the portion of the genome that was similar, indicating that these regions were likely important for adaptation to sulfidic environments. These convergent regions likely arose due to standing ancestral variation or migration. Overall, we show that extremophile populations are valuable models for addressing questions related to the colonization of novel environments.

EVOLUTIONARY GENOMICS OF ATLANTIC MOLLIES ADAPTED TO HYDROGEN-SULFIDE-RICH ENVIRONMENTS

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