Hyperdiversity of Extremotolerant Fungal Symbioses

Understanding how many species exist and the processes by which they form remains a central topic of ecological and evolutionary biology. Among the Eukaryotes, Fungi, including lichenized lineages, have given rise to unparalleled species diversity, to which it is still difficult to put firm numbers. In fact, recent studies involving molecular phylogenetic techniques have revealed an even greater or previously hidden diversity in lichens. This project takes a comprehensive approach that combines phylogenetics and population genetics tools and uses the hyperdiverse species complex Pyrenodesmia (Ascomycota) as a model organism. Previous work has suggested high levels of diversity in the extremotolerant genus Pyrenodesmia in the European Mediterranean region, whose heterogeneous landscape of complex geological and climatic history represents a globally significant hot spot of biodiversity. Yet, little is known about the influence of local ecological heterogeneity and environmental changes on the diversity of fungi, including lichens. In this project we will explore (a) whether Pyrenodesmia diversity is spatially structured in the Mediterranean and represents numerous, yet unrecognized species, (b) whether adaptation to different ecological situations is more fine-grained than previously thought, and (c) whether symbiotic partners contribute to diversification. With this project we also aim to develop a more general understanding for the evolution of extremotolerant eukaryotic microorganisms.

The fungal kingdom comprises a very diverse group of closely related organisms. They all share a relatively simple structural pattern, at the edge between what us humans perceive as microorganisms and multicellular life forms. Fungi harbour an astonishingly large functional diversity despite the slickness of their genomes, which are 100 times smaller in size than those of the simplest animals or plants. Fungi are found everywhere across the biosphere, playing very different ecological roles. The most striking pattern of fungal lineages is their tendency to cooperate with other organisms forming a sort of passive-aggressive associations that we call symbioses. Without any doubt lichens are an outstanding example of such symbioses. In them, fungi and algae establish a permanent partnership which generates a completely new form of life, which we call the lichen thallus. As Aristotle would state, the whole is greater than the sum of its parts, thus synergic lichen systems are even capable of sustaining life in Earths most extreme environments, surviving on the scarce water, mineral and light resources available. In an attempt to understand the patterns giving rise to the extreme diversity of lichen fungi, we focused in studying the lichen genus Pyrenodesmia s.s. across the Mediterranean region using molecular genetic tools. A fundamental quest in lichen research is discovering all those unknown species waiting to be seen at the other side of the magnifying glass. This quest became even more revealing when DNA tools became available for taxonomic research. And as consequence we tended to interpret most genetic diversity arising as a result of the evolution of new species. Our project found an even larger molecular diversity in Pyrenodesmia than what we had anticipated. Although we started thinking that there were hundreds of species were just a dozen was described, we developed a critical thinking and dove into the reproductive biology and the genomes of the lichen fungi under study. Under this new we came to understand that a high molecular diversity could be driven by a multiplicity of processes and mechanisms, which may be acting at different levels of organization, and not necessarily the species level. European Pyrenodesmia species form a complex evolutionary unit, which we called a meta- species. Within meta-species, species and populations are widely interconnected through sexual reproduction, but do not merge into a single hybrid. Species within a meta-species do maintain a high degree of morphological and ecological independence despite of extensive gene-flow, driven by the existence of post-reproductive barriers caused either by endogenous factors, such as functional limitations or molecular mechanisms of self- recognition, or by exogenous factors such as divergent performance across ecological gradients.