Urbanization and distance shape population structure in Fundulus heteroclitus

The federal Superfund site at New Bedford Harbor (Massachusetts, USA) is an example of an environment where pollution levels rose quickly and dramatically. Industrial waste containing polychlorinated biphenyls, heavy metals, and other organic pollutants was dumped into the harbor in the mid-20th century. The mummichog (Fundulus heteroclitus) is a widely distributed fish typically susceptible to polychlorinated biphenyl toxicity. However, the population in New Bedford Harbor is one of several that have evolved the ability to tolerate this category of toxicants. Constituents of the aryl hydrocarbon receptor system are linked to this adaptive pollution tolerance. Our population genetic analysis of 444 mummichogs from Massachusetts and Rhode Island estuaries using 55 SNP loci suggests that F. heteroclitus near New Bedford Harbor have large populations and restricted but meaningful levels of gene exchange among adjacent habitats. When comparing polluted to cleaner sites, we find strong evidence of genetic differentiation at a small geographic scale. Populations at the two most polluted sites form a genetically distinct cluster. Much of this differentiation is driven by allele frequency differences at loci associated with the aryl hydrocarbon receptor system. While allele frequencies at loci associated with pollution tolerance vary between clean and polluted habitats, putatively adaptive alleles are present at low frequency elsewhere in our study area.