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Lichen associations are overwhelmingly supported by carbon produced by photosynthetic algal symbionts. These algae have diversified to occupy nearly all climates and continents; however, we have a limited understanding of how their climatic niches have evolved through time. Here we extend previous work and ask whether phylogenetic signal in, and the evolution of, climatic niche, varies across climatic variables, phylogenetic scales, and among algal lineages in Trebouxia—the most common genus of lichen-forming algae. Our analyses reveal heterogeneous levels of phylogenetic signal across variables, and that contrasting models of evolution underlie the evolution of climatic niche divergence. Together these analyses demonstrate the variable processes responsible for shaping climatic tolerance in Trebouxia, and provide a framework within which to better understand potential responses to climate change-associated perturbations. Such predictions reveal a disturbing trend in which the pace at which modern climate change is proceeding will vastly exceed the rate at which Trebouxia climatic niches have previously evolved.

Fungal–algal relationships—both across evolutionary and ecological scales—are finely modulated by the presence of the symbionts in the environments and by the degree of selectivity and specificity that either symbiont develop reciprocally. In lichens, the green algal genus Trebouxia Puymaly is one of the most frequently recovered chlorobionts. Trebouxia species-level lineages have been recognized on the basis of their morphological and phylogenetic diversity, while their ecological preferences and distribution are still only partially unknown. We selected two cosmopolitan species complexes of lichen-forming fungi as reference models, i.e., Rhizoplaca melanophthalma and Tephromela atra, to investigate the diversity of their associated Trebouxia spp. in montane habitats across their distributional range worldwide. The greatest diversity of Trebouxia species-level lineages was recovered in the altitudinal range 1,000–2,500 m a.s.l. A total of 10 distinct Trebouxia species-level lineages were found to associate with either mycobiont, for which new photobionts are reported. One previously unrecognized Trebouxia species-level lineage was identified and is here provisionally named Trebouxia “A52.” Analyses of cell morphology and ultrastructure were performed on axenically isolated strains to fully characterize the new Trebouxia “A52” and three other previously recognized lineages, i.e., Trebouxia “A02,” T. vagua “A04,” and T. vagua “A10,” which were successfully isolated in culture during this study. The species-level diversity of Trebouxia associating with the two lichen-forming fungi in extreme habitats helps elucidate the evolutionary pathways that this lichen photobiont genus traversed to occupy varied climatic and vegetative regimes.

Lichens are classic models of symbiosis, and one of the most frequent nutritional modes among fungi. The ecologically and geographically widespread lichen-forming algal (LFA) genus Trebouxia is one of the best-studied groups of LFA and associates with over 7000 fungal species. Despite its importance, little is known about its diversification. We synthesized twenty years of publicly available data by characterizing the ecological preferences of this group and testing for time-variant shifts in climatic regimes over a distribution of trees. We found evidence for limited shifts among regimes, but that disparate lineages convergently evolved similar ecological tolerances. Early Trebouxia lineages were largely forest specialists or habitat generalists that occupied a regime whose extant members occur in moderate climates. Trebouxia then convergently diversified in non-forested habitats and expanded into regimes whose modern representatives occupy wet-warm and cool-dry climates. We rejected models in which climatic diversification slowed through time, suggesting climatic diversification is inconsistent with that expected under an adaptive radiation. In addition, we found that climatic and vegetative regime shifts broadly coincided with the evolution of biomes and associated or similar taxa. Together, our work illustrates how this keystone symbiont from an iconic symbiosis evolved to occupy diverse habitats across the globe.