Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population

Abstract

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 polychlorinated biphenyl (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) signalling 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 signalling pathways that cross-talk with AHR was implicated as one candidate mechanism for the adaptive AHR signalling 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.

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

“…However, these studies have tended to compare gene expression across taxa in static common-garden environments. In contrast, much functionally relevant variation is likely to be revealed within experimental designs that manipulate environmental conditions such that transcriptomewide norms of reaction can be compared across taxa (49)(50)(51). These designs, including the experiments presented here, promise to offer more nuanced insight into the functional relevance of genes with expression patterns that vary in response to the environment and vary across taxa from different native environments.…”

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

“…Almost no differences in constitutive gene expression were apparent between tolerant and sensitive populations during development in clean, “common‐garden” conditions (Bozinovic & Oleksiak, 2010). However, upon exposure to model toxicants, including PCBs and PAHs, large differences in inducible expression clearly distinguished tolerant fish from fish from a nearby sensitive reference population (Bozinovic et al., 2013; Oleksiak et al., 2011; Whitehead et al., 2010). These results show that the functional divergence in gene expression between populations is dependent on exposure to toxicants—an example of population‐by‐environment interaction.…”

“…For this purpose, F1 progeny were produced by cross‐breeding mature killifish from NBH and Block Island, RI, one of the most sensitive populations ever tested (Nacci et al., 2010), and when mature these F1 fish were crossed to produce F2 embryos. These F2 embryos were exposed to a single differentiating concentration of PCB126 and phenotyped during development, demonstrating their representation of the range of sensitivity between the two originating populations (e.g., Whitehead et al., 2010). F2 embryos were genotyped using a dense panel of markers including targeted SNPs (Proestou et al., 2014) and microsatellite markers (Waits et al., 2016).…”

Evolutionary toxicology in an omics world

“…On the other hand, genetic variation can alter the response of toxin activated genes and pathways (Bozinovic, Sit, Di Giulio, Wills, & Oleksiak, 2013; Reid et al., 2016; Whitehead, Pilcher, Champlin, & Nacci, 2012; Whitehead, Triant, Champlin, & Nacci, 2010). Thus, it becomes imperative to understand the genetic variation within a population and how that affects responsiveness to a specific toxin.…”

“…In populations of F. heteroclitus adapted to contaminated environments, the transcriptional profiles of control individuals are rather indistinguishable from references (Fisher & Oleksiak, 2007; Oleksiak, 2008). On the other hand, when presented with stressors, the responses of adapted populations diverge from those of references (Fisher & Oleksiak, 2007; Oleksiak, 2008; Whitehead et al., 2010). This suggests not only that there is variability in the expression of genes in response to contaminants, which is encoded genetically, but that induced expression response profiles can be altered through natural selection in contaminated environments.…”