Species evolution in symbiosis

- Evolutionary novelty is a long-term consequence of interspecific interactions. Lichens are one of the best-known examples of fungal symbioses, but the details of species evolution under conditions of symbiosis are still poorly known. Because lichens represent richly diversified fungal lineages and since they are easily recognized by the colorful and conspicuous morphology of the mycobiont, they represent well-suited models to address questions of symbiotic evolution of fungal species. Classification of lichens relies largely on morphology. According to these characters, many species are heterogeneous and represent unresolved species complexes, however, morphological classification fail to resolve species complexes and identify uniform species. Furthermore, they are not suited to understand to what extent mycobiont genotypes correlate with symbiont selectivity. In this project we aim to investigate the genetic aspects of the symbiotic speciation of lichens using taxa belonging to the cosmopolitan Tephromela atra species complex as models. We will choose a wide set of molecular markers, both for the fungal and the algal partners, which can reveal novel informative characters and provide further information to resolve species definition and phylogenetic relationships within the Tephromela atra complex. This will be further used to test whether evidence from previous studies for ongoing genetic differentiation in sympatric populations of Tephromela atra can be confirmed and extended on a worldwide scale. We will further test under controlled culture conditions the physiological performance of the algal partner, which can be a determinant of the adaptability of mycobiont species to specific ecological conditions and can influence the speciation process.

Understanding how many species exist and the processes by which they form is a central topic of ecological and evolutionary biology. For many microbial groups, however, estimation of biodiversity and the study of their evolution are special challenges. Lichens, well established and structured symbiotic associations between fungi, the mycobionts, and photosynthetic algae, the photobionts, represent one of the best examples in which patterns of high phenotypic plasticity coupled with wide geographic distributions shape species evolution and diversity. We sampled the lichen-forming species-complex Tephromela atra and related species at a world-wide scale to study the evolution of the mycobionts and the photobionts in symbiosis. We reconstructed a phylogenetic hypothesis of both bionts based on nuclear markers and we analysed morphological and chemical traits to assess how phenotypic relationships of species agrees with molecular data. We also studied the patterns of selectivity that the mycobionts present towards the photobionts by applying molecular and culture-dependent approaches. Using a phylogenetic approach and by combining morphological and chemical characters, ecological preferences and geographic origin of the lichens, we could distinguish six well-differentiated species of Tephromela mycobionts, which also present high specificity for their Trebouxia photobionts. Alternatively, the continuum of variability observed in morphology and chemical patterns in a widely ecologically distributed group of Tephoromela atra prevented us the description of new taxa with characteristic traits. The fungus T. atra presents, furthermore, low selectivity towards the photobionts, associating with seven lineages of Trebouxia. Additionally, we discovered new clades in Trebouxia, demonstrating that there is still unrecognized diversity of lichenized algae. We observed that the photobiont selectivity shape the evolution of the mycobionts and is correlated with well-resolved, monophyletic fungal clades. Alternatively, broad photobiont selectivity corresponds to poor phylogenetic resolution of the widely distributed, euryoecious mycobionts. The association with a broad range of photobionts could represent a bet-hedging strategy of the lichen mycobionts to ameliorate the effects of ecological change. Hence, lichens with ample ecological niche or wide photobiont selectivity could more likely survive ecological alterations by associating with adapted photobionts in the range of their niche. As a consequence this strategy could explain differential vulnerability of lichens to environmental change.