Common mechanism underlies repeated evolution of extreme pollution tolerance

Abstract

Human alterations to the environment can exert strong evolutionary pressures, yet contemporary adaptation to human-mediated stressors is rarely documented in wildlife populations. A common-garden experimental design was coupled with comparative transcriptomics to discover evolved mechanisms enabling three populations of killifish resident in urban estuaries to survive normally lethal pollution exposure during development, and to test whether mechanisms are unique or common across populations. We show that killifish populations from these polluted sites have independently converged on a common adaptive mechanism, despite variation in contaminant profiles among sites. These populations are united by a similarly profound desensitization of aryl-hydrocarbon receptor-mediated transcriptional activation, which is associated with extreme tolerance to the lethal effects of toxic dioxin-like pollutants. The rapid, repeated, heritable and convergent nature of evolved tolerance suggests that ancestral killifish populations harboured genotypes that enabled adaptation to twentieth-century industrial pollutants.

Incorporating evolutionary insights to improve ecotoxicology for freshwater species

“…Multidisciplinary perspectives and techniques, for example from genetics, physiology, and ecology, have yielded a robust understanding of toxicological outcomes and mechanisms across levels of biological organization, from molecular processes to population‐level and community‐level consequences (Peterson et al., 2003; Sturla et al., 2014; Whitehead, Pilcher, Champlin, & Nacci, 2012). Indeed, efforts aimed at understanding how molecular impacts of contaminants shape ecological outcomes have become a recent focus of ecotoxicology (e.g., “adverse outcome pathways,” Ankley et al., 2010).…”

Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout

“…In such cases, these parallel phenotypic changes may have the same underlying genetic basis [12 -17] or may involve different genetic changes that cause similar phenotypic responses [18,19]. While parallel adaptation may stem from novel mutations in the same gene or gene region, it is often attributed to concordant changes in the frequencies of existing alleles [14][15][16]20,21] or to parallel regulatory changes in gene expression [22,23]. However, the relative importance and frequency of these different underlying genomic responses to adaptive evolution in natural populations is largely unknown.…”

Paracellular pathway remodeling enhances sodium secretion by teleost fish in hypersaline environments

“…Karnaky (1986) focused on chloride cell structure and function in the ionocyte-rich opercular epithelium, while Wood and Marshall (1994) compared in vitro and in vivo approaches to understanding euryhalinity in teleost fishes. Recently, the species has been recognized as a valuable genomic model in physiology (Burnett et al, 2007;Whitehead, 2010;Whitehead et al, 2011a,b) and toxicology (Whitehead et al, 2012) and sequencing of the genome is complete (www.fundulus.org). Current models for teleost ion transport and acid-base regulation in gills (Evans et al, 2005) include transcellular Cl − secondary active transport in a two-step process in seawater-type NaCl-secreting ionocytes [Type IV ionocytes as per functional classification (Hiroi et al, 2005)].…”