mtDNA recombination indicative of hybridization suggest a role of the mitogenome in the adaptation of reef building corals to extreme environments

Abstract

mtDNA recombination following hybridization is rarely found in animals and was never until now reported in reef-building corals. Here we report unexpected topological incongruence among mitochondrial markers as evidence of mitochondrial introgression in the phylogenetic history of Stylophora species distributed along broad geographic ranges. Our analyses include specimens from the Indo-Pacific, the Indian Ocean and the full latitudinal (2000 km) and environmental gradient (21{degrees}C-33{degrees}C) of the Red Sea (N=827). The analysis of Stylophora lineages in the framework of the mitogenome phylogenies of the family Pocilloporidae, coupled with analyses of recombination, shows the first evidence of asymmetric patterns of introgressive hybridization associated to mitochondrial recombination in this genus. Hybridization likely occurred between an ancestral lineage restricted to the Red Sea/Gulf of Aden basins and migrants from the Indo-Pacific/Indian Ocean that reached the Gulf of Aden. The resulting hybrid lives in sympatry with the descendants of the parental Red Sea lineage, from which it inherited most of its mtDNA (except a highly variable recombinant region that includes the nd6, atp6, and mtORF genes) and expanded its range into the hottest region of the Arabian Gulf, where it is scarcely found. Noticeably, across the Red Sea both lineages exhibit striking differences in terms of phylogeographic patterns, clades-morphospecies association, and zooxanthellae composition. Our data suggest that the early colonization of the Red Sea by the ancestral lineage, which involved overcoming multiple habitat changes and extreme temperatures, resulted in changes in mitochondrial proteins, which led to its successful adaptation to the novel environmental conditions.