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

Abstract

For most species, evolutionary adaptation is not expected to be sufficiently rapid to buffer the effects of human-mediated environmental changes, including environmental pollution. Here we review how key features of populations, the characteristics of environmental pollution, and the genetic architecture underlying adaptive traits, may interact to shape the likelihood of evolutionary rescue from pollution. Large populations of Atlantic killifish (Fundulus heteroclitus) persist in some of the most contaminated estuaries of the United States, and killifish studies have provided some of the first insights into the types of genomic changes that enable rapid evolutionary rescue from complexly degraded environments. We describe how selection by industrial pollutants and other stressors has acted on multiple populations of killifish and posit that extreme nucleotide diversity uniquely positions this species for successful evolutionary adaptation. Mechanistic studies have identified some of the genetic underpinnings of adaptation to a well-studied class of toxic pollutants; however, multiple genetic regions under selection in wild populations seem to reflect more complex responses to diverse native stressors and/or compensatory responses to primary adaptation. The discovery of these pollution-adapted killifish populations suggests that the evolutionary influence of anthropogenic stressors as selective agents occurs widely. Yet adaptation to chemical pollution in terrestrial and aquatic vertebrate wildlife may rarely be a successful "solution to pollution" because potentially adaptive phenotypes may be complex and incur fitness costs, and therefore be unlikely to evolve quickly enough, especially in species with small population sizes.

Keywords: adaptation; contemporary evolution; ecological genetics; ecotoxicology; genomics/proteomics; molecular evolution; natural selection and contemporary evolution; population genetics—empirical.

Figure 1

Population variation in killifish larval survival when challenged with increasing exposure concentrations of PCB126. Modeled responses from repeated laboratory tests show that populations from polluted sites (solid curves) exhibit tolerance to pollutants at concentrations hundreds to thousands of times normally lethal levels (sensitive populations, dashed curves). Populations are indicated by colors as shown in the map, which shows locations of tolerant populations (solid circles: New Bedford Harbor [NBH], Bridgeport [BP], Newark [NWK], and Elizabeth River [ER] from north to south) and sensitive reference populations (open circles: Block Island [BI], Flax Pond [FP], Sandy Hook [SH], and Kings Creek [KC], from north to south). PCB, polychlorinated biphenyl

Figure 2

Comparison of a normally developed embryo (left) and a PCB‐affected embryo (right) at 10 days postfertilization. Exposure to dioxin‐like chemicals, including some PCBs, causes a suite of developmental effects, including reduced embryo size, swim bladder malformation, alteration of jaw cartilage, vascular hemorrhaging, pericardial and yolk‐sac edema, and malformation of the heart. On the right, a severely affected fish exhibits a heart that resembles a tube, unable to generate substantial blood flow, accompanied by massive pericardial edema. On the left, a normally developed embryo has a compact heart, with a ventricle and atrium aligned side by side under the jaw. Fish that have evolved tolerance show very limited signs of these developmental defects following chemical exposure, even at doses thousands of times higher than those that cause these effects in fish from reference (clean) sites. These developmental impacts are ultimately lethal. V, ventricle; A, atrium; PE, pericardial edema; BA, bulbus arteriosus; SV, sinus venosus; PCB, polychlorinated biphenyl

Figure 3

Differences in the transcriptional response to PCB126 exposure among northern tolerant and sensitive killifish populations. Populations indicated by colored circles (filled or open) as in Figure 1. Heatmaps show genes that differ in their response to PCB exposure. Columns are treatments, including control and exposure concentrations of PCB126 (ng/L), rows are genes, and the color of cells indicates expression relative to control (black) where yellow and blue represent up‐ and down‐regulation, respectively. Populations from reference sites show a common up‐regulation of a suite of genes that is enriched for the transcriptional targets of an activated AHR signaling pathway. Tolerant populations from polluted sites show little transcriptional response to the same exposures that cause large gene expression changes in sensitive reference fish. However, the transcriptional response of tolerant fish becomes similar to that of sensitive fish after the dose is increased two to three orders of magnitude. This demonstrates that AHR activation is profoundly desensitized, but not completely disabled, in killifish populations that have evolved pollution tolerance. PCB, polychlorinated biphenyl; AHR, aryl hydrocarbon receptor

Figure 4

Genetic markers identified as quantitative trait loci (black) associated with tolerance to dioxin‐like compounds (DLCs) in New Bedford Harbor (MA) killifish, and some candidate genes (red) known for their involvement in the aryl hydrocarbon receptor (AHR) signal transduction pathway through which DLCs act (Nacci, Proestou, et al., 2016)

Figure 5

Genomic regions showing strongest signatures of selection between tolerant‐sensitive pairs of populations are shared among tolerant populations, and include genes in the AHR signaling pathway, indicating convergent adaptation at the pathway and gene levels. However, different molecular variants are implicated in different populations. Populations indicated by colored circles (filled or open) as in Figure 1. Phylogenetic tree at the top left was estimated from genomewide bi‐allelic SNP frequencies, and shows the expected biogeographic pattern of relatedness among populations: geographically nearby populations cluster together, and northern populations are distinct from southern. The center panel illustrates the key proteins associated with the AHR signaling pathway. Among the strongest signals of selection are genes AHR,AIP, and CYP1A. For AIP, a common haplotype was favored by selection in northern populations, but a distinct haplotype diverged in the ER population (phylogenetic tree at top right). The genomic region around AHR2a and AHR1a is highly divergent between tolerant and sensitive populations, but only in the ER (red circle) population is this selection signal associated with a deletion that has swept to high frequency (bottom left panel). CYP1A falls in a region of strong selection for all tolerant populations, but only in the northern populations is this signal associated with up to eightfold duplication of the CYP 1A locus (bottom right panel). AHR, aryl hydrocarbon receptor; CYP1A, cytochrome P450 1A; AIP, AHR‐interacting protein