A novel test for significant codivergence between cool-season grasses and their symbiotic fungal endophytes

Symbioses of grasses and fungal endophytes constitute an interesting model for evolution of mutualism and parasitism. Grasses of all subfamilies can harbor systemic infections by fungi of the family Clavicipitaceae. Subfamily Poöideae is specifically associated with epichloë endophytes (species of Epichloë and their asexual derivatives, the Neotyphodium species) in intimate symbioses often characterized by highly efficient vertical transmission in seeds, and bioprotective benefits conferred by the symbionts to their hosts. These remarkable symbioses have been identified in most grass tribes spanning the taxonomic range of the subfamily. Here we examine the possibility of codivergence in the phylogenetic histories of Poöideae and epichloë. We introduce a method of analysis to detect significant codivergence even in the absence of strict cospeciation, and to address problems in previously developed methods. Relative ages of corresponding cladogenesis events were determined from ultrametric maximum likelihood H (host) and P (parasite = symbiont) trees by an algorithm called MRCALink (most recent common ancestor link), an improvement over previous methods that greatly weight deep over shallow H and P node pairs. We then compared the inferred correspondence of MRCA ages in the H and P trees to the spaces of trees estimated from 10,000 randomly generated H and P tree pairs. Analysis of the complete dataset, which included a broad host-range species and some likely host transfers (jumps), did not indicate significant codivergence. However, when likely host jumps were removed the analysis indicated highly significant codivergence. Interestingly, early cladogenesis events in the Poöideae corresponded to early cladogenesis events in epichloë, suggesting concomitant origins of the Poöideae and this unusual symbiotic system.