Introgression from extinct species facilitates adaptation to its vacated niche

Frei, David; Reichlin, Pascal; Seehausen, Ole; Feulner, Philine G. D. (2023). Introgression from extinct species facilitates adaptation to its vacated niche. Molecular Ecology, 32(4), pp. 841-853. Wiley-Blackwell 10.1111/mec.16791

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Anthropogenic disturbances of ecosystems are causing a loss of biodiversity at an
unprecedented rate. Species extinctions often leave ecological niches underutilized, and
their colonization by other species may require new adaptation. In Lake Constance, an
endemic profundal whitefish species went extinct during a period of anthropogenic
eutrophication. In the process of extinction, the deep-water species hybridized with
three surviving whitefish species of Lake Constance, resulting in introgression of genetic
variation that is potentially adaptive in deep-water habitats. Here, we sampled a water
depth gradient across a known spawning ground of one of these surviving species,
Coregonus macrophthalmus, and caught spawning individuals in greater depths (down
to 90m) than historically recorded. We sequenced a total of 96 whole genomes, 11-17 for
each of six different spawning depth populations (4m, 12m, 20m, 40m, 60m, and 90m),
to document genomic intraspecific differentiation along a water depth gradient. We
identified 52 genomic regions 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 potentially facilitates ongoing
adaptation to deep water. Our results are consistent with the syngameon hypothesis,
proposing that hybridization between members of an adaptive radiation can promote
further niche expansion and diversification. Furthermore, our findings demonstrate that
introgression from extinct into extant species can be a source of evolvability enabling
rapid adaptation to environmental change and may contribute to the ecological recovery
of ecosystem functions after extinctions.

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