Reticulate evolution and rapid development of reproductive barriers upon secondary contact pose challenges for species delineation in a forest fungus

Abstract

Reproductive barriers within morphospecies of the mushroom-forming fungi tend to be stronger between sympatric lineages, leading to speculation on whether they are being reinforced by selection against hybrids. In this study we use population genomic analyses together with in vitro crosses of a global sample of the wood decay fungus Trichaptum abietinum to investigate reproductive barriers within this morphotaxon and the processes that have shaped them. Our phylogeographic analyses show that the morphospecies is delimited into six major lineages, one in Asia, two in Europe, and three in North America. The two lineages present in Europe are interfertile and admixed, whereas our crosses show that the North American lineages are reproductively isolated. In Asia a more complex pattern appears, with partial intersterility between multiple sub-lineages that likely originated independently and more recently than the reproductive barriers in North America. We found pre-mating barriers in T. abietinum to be moderately correlated with genomic divergence, whereas fitness of the mated hybrids showed a strong positive correlation with increasing genomic divergence. Genome wide association analyses identified candidate genes with programmed cell death annotations, which are known to be involved in intersterility in distantly related fungi. Our demographic modelling and phylogenetic network analyses suggest that reproductive barriers in Trichaptum abietinum could have been reinforced upon secondary contact between lineages that diverged in allopatry during the Pleistocene glacial cycles. Our combination of experimental and genomic approaches demonstrate how T. abietinum is a tractable system for studying speciation mechanims.