Adaptive alien genes are maintained amid a vanishing introgression footprint in a sea squirt

Abstract

Abstract Human transport of species across oceans disrupts natural dispersal barriers and facilitates hybridization between previously allopatric species. The recent introduction of the North Pacific sea squirt, Ciona robusta, into the native range of the North Atlantic sea squirt, Ciona intestinalis, is a good example of this outcome. Recent studies have revealed an adaptive introgression in a single chromosomal region from the introduced into the native species. Here, we monitored this adaptive introgression over time, examining both the frequency of adaptive alleles at the core and the hitchhiking footprint in the shoulders of the introgression island by studying a thousand Ciona spp. individuals collected in 22 ports of the contact zone, 14 of which were sampled 20 generations apart. For that purpose, we developed a KASP multiplex genotyping approach, which proved effective in identifying native, nonindigenous and hybrid individuals and in detecting introgressed haplotypes. We found no early generation hybrids in the entire sample, and field observations suggest a decline in the introduced species. At the core region of the introgression sweep, where the frequency of C. robusta alleles is the highest and local adaptation genes must be, we observed stable frequencies of adaptive alien alleles in both space and time. In contrast, we observed erosion of C. robusta ancestry tracts in flanking chromosomal shoulders on the edges of the core, consistent with the second phase of a local sweep and a purge of hitchhiked incompatible mutations. We hypothesize that adaptive introgression may have modified the competition relationships between the native and invasive species in human-altered environments.