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

Biodiversity loss can occur when disturbance compromises the reproductive barriers between species, causing them to collapse into a single population through hybridization. Recent research has documented an increasing number of cases where anthropogenic environmental disturbance is associated with new hybrid populations, but 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 rivers. Ancestry structure varied dramatically across rivers, ranging from stable coexistence to clinal hybrid zones, hinting that dynamics of hybridization in this system may be environmentally dependent. In one river, we discovered that a sudden transition in patterns of hybridization coincides with its 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. We test this by sequencing mothers and embryos from sites downstream of the urbanized area, and find reduced assortative mating, in contrast to strong assortative mating in sites upstream. We document alterations of the olfactory epithelium at the same site which are consistent with chemical irritation. Taken together, our work illuminates the mechanisms linking anthropogenic disturbance to the breakdown of reproductive isolation in hybridizing species.