Increased rates of hybridization in swordtail fish are associated with water pollution

The nature of reproductive barriers which separate species is a fundamental question of evolutionary biology. Such barriers may be sensitive to environmental conditions, and recent research has documented an increasing number of cases where anthropogenic environmental disturbance is associated with new hybrid populations. However, few studies have been able to quantitatively compare potential environmental drivers and test possible mechanisms connecting interspecific hybridization to anthropogenic disturbance. Here, we combine genomic and chemical surveys to explore the loss of reproductive isolation between the sister species Xiphophorus malinche and X. birchmanni, fishes whose riverine habitat in the Sierra Madre Oriental of Mexico is increasingly impacted by human-mediated disturbance. By sequencing whole genomes of thousands of fish, we characterize the landscape of hybridization between these species in four distinct streams. Ancestry structure varied dramatically across streams, ranging from stable coexistence to clinal hybrid zones, hinting that dynamics of hybridization in this system may be environmentally dependent. In one stream, a sudden shift in patterns of hybridization coincides with the streams passage through an urbanized area, with upstream sites showing distinct ancestry clusters and downstream sites showing a swarm of hybrids with variable ancestry. Water chemistry measurements show that water quality changes significantly over this area, including in parameters known to disrupt fish olfaction and mating. We hypothesize that the hybrid swarm downstream of the town is driven by disruption of olfaction that impacts mating preferences. By sequencing mothers and embryos, we show that there is reduced assortative mating at sites downstream of the urbanized area compared to strong assortative mating at upstream sites. We identify alterations of the olfactory epithelium at the same downstream site which are consistent with chemical irritation from polluted waters. Taken together, our work illuminates the mechanisms linking anthropogenic disturbance to the breakdown of reproductive isolation in these hybridizing species.