Increased rates of hybridization in swordtails are associated with water pollution

The nature of reproductive barriers that separate species is a fundamental question in 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 inferring genome-wide ancestry in 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 the dynamics of hybridization in this system may be environmentally dependent. In one stream, a sudden shift in hybridization patterns coincides with the stream’s passage through an urbanized area, with upstream sites showing distinct ancestry clusters and downstream sites showing a swarm of hybrids with variable ancestry. By sequencing mothers and embryos, we show that assortative mating by ancestry is weakened downstream of this urbanized area. We hypothesize that the hybrid swarm downstream of the town is driven by chemical disruption of olfaction that impacts mating preferences. Water chemistry measurements show that water quality changes significantly across this 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 that are consistent with differential effects of water quality. Taken together, our work illuminates potential mechanisms linking anthropogenic disturbance to the breakdown of reproductive isolation in these hybridizing species.