Contrasting Symbiotic Patterns in Two Closely Related Lineages of Trimembered Lichens of the Genus Peltigera

Abstract

Species circumscription is key to the characterization of patterns of specificity in symbiotic systems at a macroevolutionary scale. Here, a worldwide phylogenetic framework was used to assess the biodiversity and symbiotic patterns of association among partners in trimembered lichens from the genus Peltigera, section Chloropeltigera. We sequenced six loci of the main fungal partner and performed species discovery and validation analyses to establish putative species boundaries. Single locus phylogenies were used to establish the identity of both photobionts, Nostoc (cyanobacterium) and Coccomyxa (green alga). Distribution and specificity patterns were compared to the closely related clade, section Peltidea, which includes mainly Peltigera species with trimembered thalli. For section Chloropeltigera, eight fungal species (including five newly delimited putative species) were found in association with nine Nostoc phylogroups and two Coccomyxa species. In contrast, eight fungal species (including three newly delimited putative species) in section Peltidea were found in association with only four Nostoc phylogroups and the same two Coccomyxa species as for section Chloropeltigera. This difference in cyanobiont biodiversity between these two sections can potentially be explained by a significantly higher frequency of sexual reproductive structures in species from section Chloropeltigera compared to section Peltidea. Therefore, horizontal transmission of the cyanobiont might be more prevalent in Chloropeltigera species, while vertical transmission might be more common in Peltidea species. All Peltigera species in section Chloropeltigera are generalists in their association with Nostoc compared to more specialized Peltigera species in section Peltidea. Constrained distributions of Peltigera species that associate strictly with one species of green algae (Coccomyxa subellipsoidea) indicate that the availability of the green alga and the specificity of the interaction might be important factors limiting geographic ranges of trimembered Peltigera, in addition to constraints imposed by their interaction with Nostoc partners and by climatic factors.

Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera

“…We assembled a dataset of Peltigera-Nostoc interaction pairs summing up all information from the literature for which we could confidently assess the identity of the Peltigera species and Nostoc phylogroups or haplotypes (Chagnon et al, 2018;Lu et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018O'Brien, Miadlikowska, & Lutzoni, 2005;O'Brien, Miadlikowska, & Lutzoni, 2013;Pardo De la Hoz et al, 2018). The total dataset consisted of 1,026 thalli, or interaction pairs, representing 155 Peltigera species and 95 Nostoc phylogroups or haplotypes (Tables S1 and S2).…”

“…To infer a phylogeny for the entire genus Peltigera, we gathered published data from all currently validated species (Chagnon et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018Pardo De la Hoz et al, 2018) for seven loci (ITS, nrLSU, β-tubulin, RPB1, COR1b, COR3, COR16). We selected one representative per species with the highest number of sequenced loci, or two representatives per species when sets of available loci were mostly non-overlapping between two specimens of a species.…”

“…Because each locus was analysed separately in previous studies to detect potential topological conflicts, with appropriate corrections made when needed (Chagnon et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018Pardo De la Hoz et al, 2018), we concatenated these seven loci using in-house PERL scripts (Magain, 2018). Our concatenated dataset consisted of 205 specimens and 10,064 characters.…”

“…These modules include 1-to-1 strict F I G U R E 2 Close-ups of the seven-locus chronogram of the genus Peltigera: (a) POLY clade, that is, sections Chloropeltigera, Peltidea, Phlebia and Polydactylon, and (b) PELT clade, that is, sections Horizontales, Peltigera and Retifoveatae. Branch lengths are proportional to relative time, and each terminal tip represents a species indicated on the far right, or putative species resulting from recent studies (Magain, Miadlikowska, Goffinet, et al, 2017a;Magain et al, 2018;Pardo De La Hoz et al, 2018;Miadlikowska et al, 2018). The coloured capital letters immediately to the right of the terminal branch tips represent the network modules of each species, based on results of the modularity analyses (Figure 1).…”

Peltigera hydrophila (Lecanoromycetes, Ascomycota), a new semi-aquatic cyanolichen species from Chile

“…Peltigera sp. 14 is one of the rare cases in the genus Peltigera where both symbionts are specialists and associate almost exclusively with each other (Magain et al 2017a(Magain et al , b, 2018Miadlikowska et al 2018;Pardo-De la Hoz et al 2018;Chagnon et al 2019). The mycobiont forms thalli with Nostoc phylogroup XXIII, which was also found in a single specimen of its closest relative, P. aubertii, a species also found in Chile that otherwise associates with phylogroup XXII (Magain et al 2018).…”