Increased rates of hybridization in swordtails are associated with water pollution

Abstract

Understanding the nature of reproductive barriers separating species is a fundamental goal of evolutionary biology. Such barriers may be environmentally sensitive, and recent research has documented an increasing number of cases where anthropogenic environmental disturbance is associated with hybridization. However, few studies have been able to quantify and compare potential environmental mechanisms connecting anthropogenic disturbance to hybridization. Here, we combine genomic and environmental surveys to explore the loss of reproductive isolation between Xiphophorus malinche and X. birchmanni, fishes whose riverine habitat in montane Mexico is increasingly impacted by human-mediated disturbance. By inferring genome-wide ancestry in thousands of fish, we characterize the landscape of hybridization between these sister species in four drainages. Ancestry structure varies across streams from stable coexistence to clinal hybrid zones, hinting that hybridization dynamics in this system may be environmentally dependent. In one stream, sites upstream of an urbanized area host distinct sympatric ancestry clusters, while downstream sites collapse into a hybrid swarm. By sequencing mothers and embryos, we show that assortative mating is weakened downstream of this urbanized area. We hypothesize that the downstream hybrid swarm is driven by chemical disruption of olfaction that impacts mating preferences. Water chemistry measurements show significant changes across the urbanized area, including in parameters known to disrupt fish olfaction and mating. We identify alterations of the olfactory epithelium between sites upstream and downstream of the urbanized area consistent with differential effects of water quality. Taken together, our work illuminates potential mechanisms linking anthropogenic disturbance to the breakdown of reproductive isolation.