Gulf killifish (Fundulus grandis) live in the Houston Ship Channel (Texas, USA) despite its heavy pollution from decades of industrial activity. A study in Science uses experimental and population genomic approaches to examine the molecular underpinnings of evolved pollution resistance in F. grandis by sampling populations across a pollution gradient. The findings pinpoint genetic variants introgressed recently from the geographically distant Atlantic killifish (Fundulus heteroclitus) that provide a large adaptive advantage.

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Oziolor et al. obtained fish from 12 sites along the Channel spanning the pollution gradient, from clean to extremely polluted waters. Resistance to pollution was determined by the rates of occurrence of cardiac deformities in developing embryos exposed to a range of concentrations of a model halogenated aromatic hydrocarbon (HAH). Population variation in sensitivity to HAH-induced cardiac teratogenesis correlated with the level of habitat pollution, such that populations from the most polluted sites were resistant to HAH concentrations 1,000-fold higher than normal teratogenic levels.

Crosses between sensitive and resistant populations showed that resistance is intermediate in hybrid offspring, suggesting a genetic basis for the resistance phenotype. Resistance negatively correlated with activation of the aryl hydrocarbon receptor (AHR) pathway — the experimental knockdown of which had been shown previously to protect against HAH-induced cardiac teratogenesis — and desensitization of the AHR pathway correlated with pollution levels. Taken together, these findings suggest that desensitization to HAH-induced AHR signalling underlies resistance to pollution in F. grandis.

To determine the genetic basis of the resistance phenotype, the team sequenced whole genomes from fish that were either resistant, intermediate or sensitive to pollution. Genes encoding AHR signalling regulators showed the strongest signatures of selection. Moreover, resistant fish genomes exhibited signs of a recent population decline, for example, reduced nucleotide diversity compared with sensitive fish. This decline combined with the observed evolved resistance in the presence of strong recent selection “is consistent with evolutionary rescue in polluted populations”, write the authors.

Genes encoding AHR signalling regulators showed the strongest signatures of selection

Whole-genome sequence comparison of F. grandis and Atlantic killifish (F. heteroclitus), some of which have also evolved pollution resistance, revealed evidence of recent adaptive introgression. This finding suggests that Atlantic killifish acted as the source of genetic variation enabling the evolutionary rescue of F. grandis populations from human-led environmental change. Given that the nearest F. heteroclitus populations reside >2,500 km away, making human-mediated transport the probable mechanism of introduction, this study highlights the benefit of unfragmented landscapes (allowing free movement of animals and thus genetic variation) for preserving biodiversity.