Evolution to pollution in Gulf killifish (Fundulus grandis) from Galveston Bay, TX, USA.

Abstract

Anthropogenic contamination associated with industrial activity is a widespread and active threat to the stability of organisms. The Houston Ship Channel (HSC) is one example of a heavily impacted environment, where industrial activity has contributed to extreme levels of pollution with various classes of contaminants, such as polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs), polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs). This dissertation studies the impacts of chronic multi-generational exposure to industrial contamination on the population structure, resistance and demography in a keystone coastal species – Gulf killifish (Fundulus grandis). We have characterized their sensitivity to contaminants in populations from 12 locations across Galveston Bay, as well as the contamination levels at those sites. We found a gradient of resistance that was positively correlated with contaminant concentrations. This resistance was also correlated to a suppression of the aryl hydrocarbon receptor pathway (AHR), as estimated via the activity of a down-stream regulated enzyme – cytochrome P450 1A (CYP1A). To better understand the impacts of this adaptation, we evaluated the cross-resistance and fitness cost of populations to mechanistically and environmentally relevant stressors, but we were unable to confirm any fitness costs. We showed that the heritability of this resistance is biparental and multi-generational, which suggest that this is a genetic trait. Finally, we performed a full genome resequencing of seven populations along this gradient of resistance and discovered that genomic regions under selection in adapted populations included the AHR pathway. To determine if regulatory benchmarks on the compounds driving this adaptation would protect from such events, we performed a meta-analysis of all evolutionary events to contamination with PCBs and PAHs and found several locations, in which populations have adapted at values below regulation. Here we show that Gulf killifish populations have undergone a rapid evolutionary adaptation to a gradient of anthropogenic contaminants in Galveston Bay. In addition, we suggest that evolutionary toxicology studies, as described here, can be informative for regulatory purposes for compounds that may drive population-wide change.