Abstract
BackgroundThe non-migratory killifish Fundulus heteroclitus inhabits clean and polluted environments interspersed throughout its range along the Atlantic coast of North America. Several populations of this species have successfully adapted to environments contaminated with toxic aromatic hydrocarbon pollutants such as polychlorinated biphenyls (PCBs). Previous studies suggest that the mechanism of resistance to these and other “dioxin-like compounds” (DLCs) may involve reduced signaling through the aryl hydrocarbon receptor (AHR) pathway. Here we investigated gene diversity and evidence for positive selection at three AHR-related loci (AHR1, AHR2, AHRR) in F. heteroclitus by comparing alleles from seven locations ranging over 600 km along the northeastern US, including extremely polluted and reference estuaries, with a focus on New Bedford Harbor (MA, USA), a PCB Superfund site, and nearby reference sites.ResultsWe identified 98 single nucleotide polymorphisms within three AHR-related loci among all populations, including synonymous and nonsynonymous substitutions. Haplotype distributions were spatially segregated and F-statistics suggested strong population genetic structure at these loci, consistent with previous studies showing strong population genetic structure at other F. heteroclitus loci. Genetic diversity at these three loci was not significantly different in contaminated sites as compared to reference sites. However, for AHR2 the New Bedford Harbor population had significant FST values in comparison to the nearest reference populations. Tests for positive selection revealed ten nonsynonymous polymorphisms in AHR1 and four in AHR2. Four nonsynonymous SNPs in AHR1 and three in AHR2 showed large differences in base frequency between New Bedford Harbor and its reference site. Tests for isolation-by-distance revealed evidence for non-neutral change at the AHR2 locus.ConclusionTogether, these data suggest that F. heteroclitus populations in reference and polluted sites have similar genetic diversity, providing no evidence for strong genetic bottlenecks for populations in polluted locations. However, the data provide evidence for genetic differentiation among sites, selection at specific nucleotides in AHR1 and AHR2, and specific AHR2 SNPs and haplotypes that are associated with the PCB-resistant phenotype in the New Bedford Harbor population. The results suggest that AHRs, and especially AHR2, may be important, recurring targets for selection in local adaptation to dioxin-like aromatic hydrocarbon contaminants.
Highlights
The non-migratory killifish Fundulus heteroclitus inhabits clean and polluted environments interspersed throughout its range along the Atlantic coast of North America
Based on our results and those described above [53,64,88,89], we suggest that evolution of resistance to Polychlorinated biphenyl (PCB) in fish may converge on a common target gene, AHR2, but that the specific molecular changes may differ between species, and perhaps within a species among populations that have independently evolved the resistant phenotype
Since completion of this work, through transcriptome sequencing [59], we have identified two additional aryl hydrocarbon receptor (AHR) loci in F. heteroclitus, paralogs of the AHR loci studied here. (The differences between paralog sequences are sufficiently large so that the paralogs could not have interfered with the sequencing or Single nucleotide polymorphisms (SNPs) determinations reported in this paper.) Multiple AHRs, often occurring as pairs of paralogous AHR1 and/or AHR2 forms, have been identified in other species of fish including Danio rerio, Takifugu rubripes and Tetraodon nigroviridis, Oryzias latipes, and salmonids
Summary
Recent studies (reviewed in [4,5,6]) have provided strong evidence for adaptation of fish populations to aromatic hydrocarbons such as polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polycyclic aromatic hydrocarbons (PAHs) that cause toxicity similar to that caused by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). These “dioxin-like compounds” (DLCs) are capable of interfering with embryonic development and eliciting acute and chronic effects on reproduction, immune function, and other essential processes [7,8] with population-level consequences [9]
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