Introgression from extinct species facilitates adaptation to its vacated niche

Human alteration of ecosystems and anthropogenic environmental change are causing the loss of biodiversity at an unprecedented rate. The extinction of species often leaves ecological niches underutilized, and their colonization by other extant or new species may require novel adaptations. In Lake Constance, an endemic profundal whitefish species went extinct during a period of anthropogenic eutrophication between ~1950 and ~2000. In the process of its extinction, the deep-water species extensively hybridized with the three surviving Lake Constance whitefish species, resulting in introgression of genetic variation that is potentially adaptive in deep-water habitats. One of the surviving whitefish species, C. macrophthalmus, has recently started to expand into greater depth than historically recorded. Here we asked if it is currently adapting to the deep-water environment and if admixture variation introgressed from the extinct species may contribute. We sampled a water depth transect across a known spawning ground that includes the deepest known current whitefish spawning site in Lake Constance. We caught spawning individuals in much greater depths (90m) than previously reported for this species. We sequenced 11-17 whole genomes of fish sampled at each of six different water depths (4m, 12m, 20m, 40m, 60m and 90m). We document morphological and genomic intraspecific differentiation within C. macrophthalmus along the water depth gradient. While genome-wide differentiation along the spawning depth gradient was absent, we identified 52 regions in the genome that are potentially under divergent selection between the deepest (90m) and all shallower (4-60m) spawning habitats. At 12 (23.1%) of these 52 loci, the allele frequency pattern across historical and contemporary populations suggests that introgression from the extinct species may currently facilitate ongoing adaptation to deep water. Our results are consistent with the syngameon hypothesis of adaptive radiation, proposing that hybridization between members of an adaptive radiation can promote further niche expansion and diversification. Furthermore, our findings demonstrate that genetic variation from extinct species, maintained after historical introgression into extant species, can be an important source of evolvability under environmental change and may contribute to ecological resilience or recovery of ecosystem functions after extinctions.