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Mitochondrial Fitness, Gene Expression, and Hypoxic Stress in a Hybrid Population of the Killifish, Fundulus Heteroclitus
Citation:
FLIGHT, P. A., D. E. NACCI, D. M. CHAMPLIN, A. WHITEHEAD, AND D. RAND. Mitochondrial Fitness, Gene Expression, and Hypoxic Stress in a Hybrid Population of the Killifish, Fundulus Heteroclitus. MOLECULAR ECOLOGY. Blackwell Publishing, Malden, MA, 20(21):4503-4520, (2011).
Impact/Purpose:
This manuscript describes experimental studies that contribute to our understanding of the ecological risks associated with human-mediated stressors. Here, we assessed genome wide expression patterns, or transcriptomics, in response to an important environmental stressor, low dissolved oxygen. We used laboratory studies to characterize variation in gene expression among fish from wild populations, hypothesizing that co-existing genotypes might vary in their sensitivity to low dissolved oxygen. Results of these studies demonstrate the value of comparative transcriptomics to diagnose and predict effects of ecological stressors and characterize the mechanisms and costs of compensatory responses to such stressors by wild populations. General impacts from this contribution include improved understanding by managers and scientists of links between human activities, natural dynamics, ecological stressors and ecosystem condition.
Description:
The physiological link between oxygen availability and mitochondrial function is well established. However, whether or not fitness variation is associated with mitochondrial genotypes in the field remains a contested topic in evolutionary biology. In this study we draw on a population of the teleost fish, Fundulus heteroclitus, where functionally distinct subspecies hybridize, likely as a result of past glacial events. We had three specific aims: 1) to infer the age of the split between the subspecies using mtDNA sequences, 2) to determine the effect of mtDNA genotype on survivorship of male and female fish under hypoxic stress, 3) to determine the effect of hypoxic stress, sex and mtDNA type on gene expression. Our results are consistent with previous studies suggesting the split between F. heteroclitus is more than an order of magnitude older than the last glacial maximum. We found an unexpected and highly significant effect of sex on survivorship under hypoxic conditions, but no significant effect of mtDNA genotype. Gene expression analyses revealed hundreds of transcripts differentially regulated by sex and hypoxia. Mitochondrial transcripts and other predicted pathways were among those influenced by hypoxic stress, and a transcript corresponding to the mtDNA control region was the most highly suppressed transcript under conditions of hypoxia. Effects of mtDNA sequence variation on genome expression were limited; however a potentially important epistasis between mtDNA sequence and expression of a nuclear-encoded mitochondrial translation protein was discovered. Overall, these results confirm that mitochondrial regulation is a major component of hypoxia tolerance and further suggest that purifying selection has been the predominant selective force on mitochondrial genomes in these two subspecies.