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Comparative Transcriptomics Implicates Mechansims of Evolved Pollution Tolerance in a Killifish Population
Citation:
Whitehead, A., D. Triant, D. M. CHAMPLIN, AND D. E. NACCI. Comparative Transcriptomics Implicates Mechansims of Evolved Pollution Tolerance in a Killifish Population. MOLECULAR ECOLOGY. Blackwell Publishing, Malden, MA, 19(23):5186-5203, (2010).
Impact/Purpose:
This manuscript describes experimental studies that contribute to our understanding of the ecological risks associated with chronic contaminant exposures to wildlife populations. Here, we assessed genome wide expression patterns, or transcriptomics, in response to an important class of environmental pollutants to which tolerance has evolved in an estuarine fish species resident to estuaries of the Atlantic U.S. coast. We used laboratory studies to characterize variation in gene expression among laboratory-reared progeny of fish from populations known to vary in their sensitivity to certain pollutants to infer mechanisms of toxicity and tolerance. Results of these studies demonstrate the value of comparative transcriptomics to diagnose and predict effects of chemical stressors and characterize the mechanisms and costs of toxic and compensatory responses to chemical 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:
Wild populations of the killifish Fundulus heteroclitus resident in heavily contaminated North American Atlantic coast estuaries have recently and independently evolved dramatic, heritable, and adaptive pollution tolerance. We compared physiological and transcriptome responses to embryonic PCB exposures between one tolerant population and a nearby sensitive population to gain insight into genomic, physiological and biochemical mechanisms of evolved tolerance in killifish, which are currently unknown. The PCB exposure concentrations at which developmental toxicity emerged, the range of developmental abnormalities exhibited, and global as well as specific gene expression patterns were profoundly different between populations. In the sensitive population PCB exposures produced dramatic, dose-dependent toxic effects, concurrent with the alterations in the expression of many genes. For example, PCB-mediated cardiovascular system failure was associated with the altered expression of cardiomyocyte genes, consistent with sarcomere mis-assembly. In contrast, genome-wide expression was comparatively refractory to PCB induction in the tolerant population. Tolerance was associated with the global blockade of the aryl hydrocarbon receptor (AHR) signaling pathway, the key mediator of PCB toxicity, in contrast to the strong dose-dependent up-regulation of AHR pathway elements observed in the sensitive population. Altered regulation of signaling pathways that cross-talk with AHR was implicated as one candidate mechanism for the adaptive AHR signaling repression and the pollution tolerance that it affords. In addition to revealing mechanisms of PCB toxicity and tolerance, this study demonstrates the value of comparative transcriptomics to explore molecular mechanisms of stress response and evolved adaptive differences among wild populations.