Diversity trends of bryophytes in Antarctica are the result of adaptation, evolution and survival (including cryptobiosis): the case study of the phylogeny of Bryum argenteum

Terrestrial vegetation communities in Antarctica are predominantly composed by bryophytes and lichens, as the extreme climatic conditions of this remote continent limit the colonization of vascular plants to 2 species in the Antarctic Peninsula. A decline in bryophyte species richness occurs with latitude across the sub-Antarctic islands, Antarctic Peninsula and Antarctic continent, with a clear continent-Antarctic Peninsula separation, consistent with the Gressitt Line, a boundary identified for the invertebrate fauna, and now demonstrated also for bryophytes, suggesting a common feature in the evolutionary history of the vegetation and invertebrate fauna. Within continental Antarctica, the highest bryophyte diversity occurs in the Ross sector, despite its location is the least favorable for species migrating from the southern Hemisphere continents. Moreover, the occurrence in Antarctica of cosmopolitan species, such as Bryum argenteum, further highlights the need to understand the origin and evolution of the Antarctic flora and to investigate the role of Antarctica in explaining the dispersal routes of taxa with transoceanic or transcontinental disjunctions, with B. argenteum being an ideal target species. We reconstructed the phylogeny and divergence times of B. argenteum, both at global scale and focusing within Antarctica and Southern Hemisphere, using the nrITS region from more than 200 samples applying a molecular clock based on previously estimated substitution rates for mosses. Our analyses indicate that the distribution patterns of B. argenteum, at global scale, are the result of major paleoclimatic events occurring across the planet, and involving differentiation and migration/colonization during periods warmer than today since the Mid Miocene Climate Optimum (MMCO), as well as fragmentation during severe cooling, such as during the extensive Antarctic glaciations in the mid Miocene 14 Ma. Bryum argenteum first extensively colonized Antarctica around 9.77 Ma during the warm Tortonian (Miocene), using an intra-Antarctic dispersal route after reaching Antarctica from South America, moving the length of the Antarctic Peninsula, and reaching continental Antarctica along the coast or through inland mountains as far as Victoria Land (Ross sector), where it survived glaciations in nunataks regions that have remained ice-free for ≥ 5 My. One potential survival mechanisms during glaciations involved cryptobiosis under cold-based glaciers. Cryptobiosis is a reversible ametabolic state of life characterized by the ceasing of all metabolic processes, allowing survival of periods of intense adverse conditions. In the Antarctic Peninsula we demonstrated that entire moss individuals, dated by 14C, survived through cryptobiosis during six centuries of cold-based glacier burial in Antarctica, and that after re-exposure due to glacier retreat these mosses were able to return to a metabolically active state and remain alive. The case study of B. argenteum allows to demonstrate that Antarctica was colonized several times and that migrations occurred globally during periods of climatic optima in the Miocene and Pliocene, thus providing an analogue for biotic responses in a future warming world, in particular demonstrating the potential for future biological invasions in Antarctica.