The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish

Abstract

Atlantic killifish populations have rapidly adapted to normally lethal levels of pollution in four urban estuaries. Through analysis of 384 whole killifish genome sequences and comparative transcriptomics in four pairs of sensitive and tolerant populations, we identify the aryl hydrocarbon receptor-based signaling pathway as a shared target of selection. This suggests evolutionary constraint on adaptive solutions to complex toxicant mixtures at each site. However, distinct molecular variants apparently contribute to adaptive pathway modification among tolerant populations. Selection also targets other toxicity-mediating genes, and genes of connected signaling pathways, indicating complex tolerance phenotypes and potentially compensatory adaptations. Molecular changes are consistent with selection on standing genetic variation. In killifish high nucleotide diversity has likely been a crucial substrate for selective sweeps to propel rapid adaptation.

Evolutionary toxicology: Toward a unified understanding of life's response to toxic chemicals

“…For example, theoretical and analytical studies have developed and incorporated evolutionary techniques for ecotoxicology (e.g., Bélanger‐Deschênes et al., 2013; Klerks, Xie, & Levinton, 2011) while conceptual studies have developed frameworks for integrating evolution and ecotoxicology (e.g., Leung et al., 2017). Empirical studies have increasingly been detecting evolutionary responses in diverse environmental contexts, for example, in response to mining effluents and industrial pollutants (Bougas et al., 2016; Chen et al., 2015; García‐Balboa et al., 2013; Laporte et al., 2016; Reid et al., 2016). Studies are also beginning to show that adaptation to toxicants can evolve at a cost, for example, in the form of increased sensitivity to oxidative stress following adaptation to PCBs (Harbeitner, Hahn, & Timme‐Laragy, 2013).…”

Evolutionary toxicology in an omics world

“…Population resequencing allows for full comparisons between populations at each nucleotide, which gives it enormous power for analyzing population structure, demography, divergence, and identifying specific sequences associated with resistant phenotypes. Such projects are currently underway in both Fundulus heteroclitus (Reid et al., 2016) and F. grandis , and represent one of the most in‐depth approaches in evolutionary toxicology. The power of this approach is exemplified in a recent study of aging in turquoise killifish, Nothobranchius furzeri , which identified the specific genes responsible for an incredibly rapid generation turnover in this fish (Valenzano et al., 2015).…”

“…Studies suggest that in order to be able to predict many population‐wide statistics with power, at least 20–30 individuals per population need to be sequenced in order to reliably measure heterozygosity and to test for Hardy–Weinberg equilibrium at all loci (Luikart et al., 2003). On the other hand, the specific genetic changes of very recent selective sweeps are unavoidably difficult to pinpoint even with full‐genome population resequencing (Reid et al., 2016). Such sweeps result in portions of the genome to appear to be under selection because of genetic hitchhiking surrounding the causative region.…”

“…Such sweeps result in portions of the genome to appear to be under selection because of genetic hitchhiking surrounding the causative region. Thus, even with large sample size and coverage, the specific genes, rather than regions under selection, will prove difficult to find and are only obvious in rare cases (Reid et al., 2016). …”

“…A detailed review of evolutionary processes in response to variable stressors as studied with multigenerational genomic population resequencing can be seen in Barrick and Lenski (2013). In addition to experimental evolution, some studies found specific mutated genes and regions under selection (provided large enough coverage of sequencing) in wild populations with variable resistance due to adaptation to contamination (Reid et al., 2016). While these studies are not capable of inferring gene–gene interactions that may contribute to resistance as well as QTL studies, they have the ability to elucidate the variability in sequences that lead to differential sensitivity to contaminants, including their fixation in populations (Reid et al., 2016).…”