No need for stepping stones: Direct, joint dispersal of the lichen-forming fungus Mastodia tessellata (Ascomycota) and its photobiont explains their bipolar distribution

Aim The hypotheses proposed to explain the high percentage of bipolar lichens in Antarctica have never been explicitly tested. We used the strictly bipolar, coastal lichenized fungus Mastodia tessellata (Verrucariaceae, Ascomycota) and its photobionts (Prasiola, Trebouxiophyceae, Chlorophyta) as model species to discern whether this extraordinary disjunction originated from vicariance or long-distance dispersal. Location Coasts of Antarctica, Tierra del Fuego (Chile), Alaska (USA) and British Columbia (Canada). Methods Based on a comprehensive geographical (315 specimens and 16 populations from Antarctica, Tierra del Fuego and North America) and molecular sampling (three and four loci for the fungus and algae respectively), we implemented explicit Bayesian methods to compare alternative hypotheses of speciation and migration, and performed dating analyses for the fungal and algal partner, in order to infer the timing of the colonization events and the direction of gene flow among distant, disjunct areas. Results Mastodia tessellata comprises two fungal species which in turn associate with three photobiont lineages along the studied distribution range. Independent estimation of divergence ages for myco- and photobionts indicated a middle to latest Miocene species split in the Southern Hemisphere, and a late Miocene to Pleistocene acquisition of the bipolar distribution. Comparison of migration models and genetic diversity patterns suggested an austral origin for the bipolar species. Main conclusions The complex evolutionary history of Mastodia tessellata s.l. can be explained by a combination of vicariant and long-distance dispersal mechanisms. We provide novel evidence of a pre-Pleistocene long-term evolution of lichens in Antarctica as well as for bipolar distributions shaped by Southern to Northern Hemisphere migratory routes without the need for stepping stones.

Funding information: Spanish Ministries of Education and Economy and Competitiveness, Grant/Award Number: CTM2012-38222-C02-02, CTM2015-64728-C2-2-R, FPU AP2012-3556, RYC-2014-16784

Peer Reviewed