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

Introgressive hybridization, as evidenced by topological incongruence between nuclear and mitochondrial phylogenies, has been broadly recorded in a range of organisms. However, 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 in the phylogenetic analysis of Stylophora species distributed along broad geographic ranges, including the full latitudinal (2000 km) and environmental gradient (21°C-33°C) of the Red Sea. The analysis of Stylophora lineages in the framework of the mitogenome phylogenies of members 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 occurs in sympatry with the parental Red Sea lineage, from which it inherited most of its mtDNA (except the recombinant region that includes the nd6 , atp6 and mt ORF genes) and expanded its range into the hottest region of the Arabian Gulf. Noticeably, across the Red Sea, both lineages exhibit striking differences in terms of phylogenetic and phylogeographic patterns, clades-morphospecies association, and zooxanthellae composition. Our data suggest that the colonization of the Red Sea by the ancestral lineage, which involved overcoming the extreme temperatures of the southern Red Sea, likely resulted in changes in mitochondrial proteins, which led to its successful adaptation to the novel environmental conditions.