Do Photobiont Switch and Cephalodia Emancipation Act as Evolutionary Drivers in the Lichen Symbiosis? A Case Study in the Pannariaceae (Peltigerales)

<div><p>Lichen symbioses in the Pannariaceae associate an ascomycete and either cyanobacteria alone (usually <i>Nostoc</i>; bipartite thalli) or green algae and cyanobacteria (cyanobacteria being located in dedicated structures called cephalodia; tripartite thalli) as photosynthetic partners (photobionts). In bipartite thalli, cyanobacteria can either be restricted to a well-delimited layer within the thallus (‘pannarioid’ thalli) or spread over the thallus that becomes gelatinous when wet (‘collematoid’ thalli). We studied the collematoid genera <i>Kroswia</i> and <i>Physma</i> and an undescribed tripartite species along with representatives of the pannarioid genera <i>Fuscopannaria</i>, <i>Pannaria</i> and <i>Parmeliella</i>. Molecular inferences from 4 loci for the fungus and 1 locus for the photobiont and statistical analyses within a phylogenetic framework support the following: (a) several switches from pannarioid to collematoid thalli occured and are correlated with photobiont switches; the collematoid genus <i>Kroswia</i> is nested within the pannarioid genus <i>Fuscopannaria</i> and the collematoid genus <i>Physma</i> is sister to the pannarioid <i>Parmeliella mariana</i> group; (b) <i>Nostoc</i> associated with collematoid thalli in the Pannariaceae are related to that of the Collemataceae (which contains only collematoid thalli), and never associated with pannarioid thalli; <i>Nostoc</i> associated with pannarioid thalli also associate in other families with similar morphology; (c) ancestors of several lineages in the Pannariaceae developed tripartite thalli, bipartite thalli probably resulting from cephalodia emancipation from tripartite thalli which eventually evolved and diverged, as suggested by the same <i>Nostoc</i> present in the collematoid genus <i>Physma</i> and in the cephalodia of a closely related tripartite species; Photobiont switches and cephalodia emancipation followed by divergence are thus suspected to act as evolutionary drivers in the family Pannariaceae.</p>