Evolution of specificity in the lichen-forming genus Peltigera and its cyanobacterial partner: consequences on speciation rate and geographical range.

Variation in specificity among symbiotic partners is key to a comprehensive understanding of the evolution of symbiotic systems. This variation is expected to occur within species as well as within a broader inter- species phylogenetic framework. We assessed the level of specificity of lichen-forming Peltigera species of the section Polydactylon (mycobiont) and their cyanobacterial partner Nostoc (cyanobiont), by inferring the phylogeny of the mycobiont, based on eight nuclear loci, including three newly-developed intergenic spacers (IGS), and of their respective cyanobionts, using the rbcLX region. A total of 208 lichen thalli, representing ca. 40 putative Peltigera species, were sampled worldwide. We delimited mycobiont species using five different species delimitation methods (Structurama, bGMYC, bPTP, spedeSTEM and bPP) and circumscribed cyanobiont phylogroups based on strongly supported monophyletic groups. We found a broad spectrum of specificity for both partners, ranging from strict specialists to generalists. However, mycobionts are usually more specialized than cyanobionts by associating mostly with one or a few Nostoc phylogroups, whereas cyanobionts associate frequently with several Peltigera species. A relatively recent colonization of a new geographic area (South America) seems correlated with a switch to a generalist pattern of association by the mycobiont, and an increased rate of diversification. Specialization of the mycobiont seems to be acquired through time, i.e., favored in areas where species have been established for long periods of time, and to be associated with lower mycobiont genetic diversity. Overall, geographic ranges of these Peltigera species increase with the number of phylogroups with which they can form successful symbioses. Therefore, the evolution of specificity seems to play a key role in defining the geographical range of mycobiont species and cyanobiont phylogroups, and in mediating shifts in diversification rates of these Peltigera species.