Evolution 2019: Evolutionary Rescue from Extreme Environmental Pollution Enabled by Recent Adaptive Introgression of Highly Advantageous Haplotypes

Humans often drive quick and pronounced changes to the environment. When faced with novel environmental stressors, natural populations must adapt to changing conditions, migrate to a new location to avoid the stressors, or face extinction. Adaptation to stressful environments can arise through a number of mechanisms. First, populations can adapt using genetic variation already present in the population, provided some of this variation confers a fitness advantage in the new environment. Second, beneficial mutations may arise following the onset of the stressor and allow populations to persist. Finally, hybridization between closely related species can lead to the movement of adaptive genetic material (termed adaptive introgression) from one species to another, thereby rescuing the population from decline. Quantifying the relative importance of these different mechanisms in facilitating adaptation to novel environments would greatly improve our understanding of how populations cope with rapid environmental change.

In his talk at Evolution 2019, professor Andrew Whitehead from the University of California Davis’ Department of Environmental Toxicology examined the genetic basis of resistance to toxic water pollutants in populations of the Gulf Killifish (Fundulus grandis) along the northern Gulf of Mexico. Many decades of heavy industrial activity through the Houston Ship Channel have created a gradient in the concentration of toxic halogenated and polycyclic aromatic hydrocarbons (HAHs and PAHs), which cause cardiac defects in developing fish and reduce fitness. Fish from the most polluted sites are able to tolerate toxic HAHs at levels approximately 1000 times that of fish from less polluted sites, suggesting evolved resistance to the damaging effects of environmental pollutants. Additionally, fish from polluted sites have greater desensitisation of the Aryl hydrocarbon receptor (AHR) signaling pathway, which mediates the HAH-induced cardiac defects and suggests AHR plays an important role in the evolution of resistance in these populations.

To identify the genetic basis of resistance, Whitehead and colleagues sequenced the genomes of fish from populations along the contamination gradient. Scanning across the genomes, they found evidence of natural selection targeting genes in the AHR signaling pathway, in addition to genes coding for proteins that interact with AHR gene products and facilitate their activity. The desensitisation of AHR in resistant populations results from a large genomic deletion in the AHR pathway, the frequency of which scales with resistance (i.e. highest in most resistant populations and lowest in the least resistant populations). Interestingly, this resistance-conferring deletion appears to have introgressed into Gulf Killifish populations from the closely related Atlantic Killifish (Fundulus heteroclitus) that spans the eastern coast of North America: modeling showed this introgression occurred approximately 34 generations ago (i.e., after the split between the two killifish species) and that it confers a very large fitness advantage to resident Gulf Killifish individuals. Given the geographic distance between Gulf and Atlantic Killifish, human-mediated transport of Atlantic Killifish into the Gulf of Mexico is a likely avenue by which this introgression occurred. This work highlights adaptive introgression through hybridization as an important mechanism allowing the population to adapt to rapid and pressing environmental change. This work was recently published in the journal Science. You can read more about work from the Whitehead lab here.

 

You can watch the full presentation here:

 

Featured image: Andrew Whitehead, a professor at the University of California Davis in the Department of Environmental Toxicology, presents work from his group’s recent Science paper at the 2019 Evolution conference in Providence, RI.

James Santangelo

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