Neogene speciation and Pleistocene expansion of the genus Pseudephebe (Parmeliaceae, lichenized fungi) involving multiple colonizations of Antarctica.

Widespread geographic distributions in lichens have been usually explained by the high dispersal capacity of their tiny diaspores. However, recent phylogenetic surveys have challenged this assumption and provided compelling evidence for cryptic speciation and more restricted distribution ranges in diverse lineages of lichen-forming fungi. To evaluate these scenarios, we focus on the fungal genus Pseudephebe (Parmeliaceae) which includes amphitropical species, a distribution pattern whose origin has been a matter of debate since first recognized in the nineteenth century. In our study, a six-locus dataset and a broad specimen sampling covering almost all Earth's continents is used to investigate species delimitation in Pseudephebe. Population structure, gene flow and dating analyses, as well as genealogical reconstruction methods, are employed to disentangle the most plausible transcontinental migration routes, and estimate the timing of the origin of the amphitropical distribution and the Antarctic populations. Our results demonstrate the existence of three partly admixed phylogenetic species that diverged between the Miocene and Pliocene, and whose Quaternary distribution has been strongly driven by glacial cycles. Pseudephebe minuscula is the only species showing an amphitropical distribution, with populations in Antarctica, whereas the restricted distribution of P. pubescens and an undescribed Alaskan species might reflect the survival of these species in European and North American refugia. Our microevolutionary analyses suggest a Northern Hemisphere origin for P. minuscula, which could have dispersed into the Southern Hemisphere directly and/or through "mountain-hopping" during the Pleistocene. The Antarctic populations of this species are sorted into two genetic clusters: populations of the Antarctic Peninsula were grouped together with South American ones, and the Antarctic Continental populations formed a second cluster with Bolivian and Svalbard populations. Therefore, our data strongly suggest that the current distribution of P. minuscula in Antarctica is the outcome of multiple, recent colonizations. In conclusion, our results stress the need for integrating species delimitation and population analyses to properly approach historical biogeography in lichen-forming fungi.

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