The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi

Abstract

Aim: Achlorophyllous mycoheterotrophic plants and mycorrhizal fungi often have highly specific interactions that potentially limit the plants’ distribution and diversification potential. However, specificity in biotic interactions may differ considerably over a species’ distribution range and therefore interactions need to be studied over their entire range to assess their evolution in space and time. The present study investigates the biogeographical history of the interaction between five closely related mycoheterotrophic Thismia species and arbuscular mycorrhizal fungi over the distribution range of the plant species. Location: Temperate south-east Australia and New Zealand. Methods: Phylogenetic relationships of Thismia (nrITS and mtcob) and their arbuscular mycorrhizal fungi (partial nrSSU) were reconstructed based on data from 65 plant specimens. The diversification times in Thismia were estimated with a Bayesian relaxed clock approach using a Dioscoreales framework (nrSSU, mtatp1, mtmatR, mtnad1 b-c). Ancestral geographical ranges were reconstructed using a maximum likelihood approach. The same approach was used to reconstruct ancestral mycorrhizal associations. Results: Our analysis shows that Thismia plants have highly specific, phylogenetically conserved and evolutionarily persistent interactions with Rhizophagus fungi. Nevertheless, Thismia was able to diversify and radiate recently due to the wide geographical distribution of the host fungi. In addition, we find that although the mycorrhizal interactions of this clade of mycoheterotrophs are strictly bound to a fungal lineage, host switches remain possible. Main conclusions: In this clade of closely related mycoheterotrophs, dependency on highly specific fungal interactions is the result of phylogenetic niche conservatism, acting over at least 12 million years. Nevertheless, plants that are dependent on highly specific fungal interactions have ample opportunities to disperse and radiate over the geographical range of their hosts. Our study highlights the need to link the ecology and evolution of species interactions over broad geographical and evolutionary scales for understanding mycorrhizal interactions.