Convergent evolution of a symbiotic duet: The case of the lichen genus Polychidium (Peltigerales, Ascomycota)

Abstract

Thallus architecture has long been a powerful guide for classifying lichens and has often trumped photobiont association and ascomatal type, but the reliability of these characters to predict phylogenetic affinity has seldom been tested. The cyanolichen genus Polychidium unites species that have strikingly similar gross morphology but consort with different photobiont genera. If Polychidium were found to be monophyletic, photobiont switching among closely related species would be suggested. If, however, species were found to arise in different lineages, a convergent body plan and ascomatal type evolution would be inferred. We tested the monophyly of Polychidium with a multilocus phylogeny based on nuclear and mitochondrial sequence data from all known Peltigeralean families and reconstructed ancestral states for specific thallus architecture and ascomatal ontogeny types relative to Polychidium and other clades. We found that Polychidium consists of two species groups that arose independently in different suborders within the Peltigerales, associated with Nostoc and Scytonema photobionts, respectively. We infer from ancestral character state reconstruction that dendroid thallus architecture evolved independently in these two lineages. The independent development of similar dendroid thallus architecture in different fungal suborders with different photobionts represents a clear and previously overlooked example of convergent evolution in lichens. Our results also suggest a pattern of character state conservation, loss, and reversion in ascomatal ontogeny types, hitherto considered conserved traits useful for higher level ascomycete systematics.