Abstract
Populations of the non-migratory estuarine fish Fundulus heteroclitus inhabiting the heavily polluted New Bedford Harbour (NBH) estuary have shown inherited tolerance to local pollutants introduced to their habitats in the past 100 years. Here we examine two questions: (i) Is there pollution-driven selection on the mitochondrial genome across a fine geographical scale? and (ii) What is the pattern of migration among sites spanning a strong pollution gradient? Whole mitochondrial genomes were analysed for 133 F. heteroclitus from seven nearby collection sites: four sites along the NBH pollution cline (approx. 5 km distance), which had pollution-adapted fish, as well as one site adjacent to the pollution cline and two relatively unpolluted sites about 30 km away, which had pollution-sensitive fish. Additionally, we used microsatellite analyses to quantify genetic variation over three F. heteroclitus generations in both pollution-adapted and sensitive individuals collected from two sites at two different time points (1999/2000 and 2007/2008). Our results show no evidence for a selective sweep of mtDNA in the polluted sites. Moreover, mtDNA analyses revealed that both pollution-adapted and sensitive populations harbour similar levels of genetic diversity. We observed a high level of non-synonymous mutations in the most polluted site. This is probably associated with a reduction in Ne and concomitant weakening of purifying selection, a demographic expansion following a pollution-related bottleneck or increased mutation rates. Our demographic analyses suggest that isolation by distance influences the distribution of mtDNA genetic variation between the pollution cline and the clean populations at broad spatial scales. At finer scales, population structure is patchy, and neither spatial distance, pollution concentration or pollution tolerance is a good predictor of mtDNA variation. Lastly, microsatellite analyses revealed stable population structure over the last decade.
Highlights
Worldwide, anthropogenic activities have resulted in drastic ecosystem changes [1] and introduced novel stressors to natural populations
Any sequence showing more than 1% missing data was removed from the analysis
Removal of singletons weakens the power of neutrality statistics that depend on the site frequency spectrum (e.g. Tajima’s D) [41]; as such, we refrained from using these kinds of statistics on our data
Summary
Anthropogenic activities have resulted in drastic ecosystem changes [1] and introduced novel stressors to natural populations. Populations of the marine teleost Fundulus heteroclitus have adapted to anthropogenic contaminants, and embryos from populations inhabiting heavily polluted estuaries show heritable resistance to persistent organic pollutants [2] This resistance is not found in embryos from populations inhabiting relatively uncontaminated areas [2,3,4,5,6]. Reid et al [12] showed that pollution-adapted populations living in the most polluted area of the NBH estuary were independently derived from the local gene pool of nonadapted populations (i.e. adapted from standing genetic variation) This process reduced the polluted population’s effective population size (Ne) relative to neighbouring unpolluted areas. Recent work by Du [13] has shown that, for populations across NBH’s pollution cline, allele frequencies of nuclear loci covary significantly in response to the concentration of sediment pollution. These studies illustrate that genetic responses to pollution in NBH are proportional to polluting agent concentration
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