Using phylogenies of pheromone receptor genes in the Microbotryum violaceum species complex to investigate possible speciation by hybridization

Abstract

Several cases of speciation by hybridization have been reported in fungi, mostly involving recent hybridization between closely related species. In the basidiomycete genus Microbotryum by contrast some species were suspected to have arisen by hybridization between moderately distant species. In particular two species, M. lagerheimii and M. silenes-acaulis, had different placements in phylogenetic trees depending on the genes considered. Microbotryum species exhibit bipolar heterothallism, and here we analyzed sequences of the two alternate pheromone receptors to obtain further insights on the occurrence of hybridization. Indeed because mating-type loci are always heterozygous homoploid hybrid speciation should leave a permanent footprint at the mating-type locus by retaining the alternate alleles from their respective parental species. The trees obtained with each of the two pheromone receptors were well resolved, and the species relationships were in agreement with published phylogenies. Fungal pheromone receptor genes of basidiomycetes thus appear useful for phylogenetic studies, although it may not be true for the homobasidiomycetes where duplications of these genes have occurred. Furthermore an incongruence between the phylogenies of the two pheromone receptors was found for one species, M. lagerheimii, as previously observed between other nuclear genes. However additional species analyzed here revealed that the incongruence involved the whole clade including both M. lagerheimii and the Microbotryum species parasitizing Lychnis flos-cucucli. The ancestor of these species thus possibly arose via hybridization between distant ancestral lineages, although further studies should address alternative hypotheses, such as chance events during lineage sorting.

• homoploid speciation
• incomplete lineage sorting
• introgression
• mating type
• novel host
• STE3-like pheromone receptors

We thank G. Refrégier, P. Gladieux, M. Le Gac and two anonymous reviewers for comments on the manuscript. We also thank J. Abbate for providing some of the DNA and A. Gautier for her help with sequencing. We acknowledge grants ANR 06-BLAN-0201, ANR 07-BDIV-003 and ANR-09-0064-01 to TG and award of DEB-0747222 to MEH from the National Science Foundation.