Introgressive descent and hypersexuality drive the evolution of sexual parasitism and morphological reduction in a fungal species complex.

Abstract

Taxonomists consider species as discrete units of biological organization, which are subject to a continuous process of evolutionary change and are connected through their shared ancestry. However, the continuous nature of evolutionary change is difficult to reconcile with the discrete outcome of speciation, especially where species boundaries are permeable. A good example of this inconsistency is the lichen genus Pyrenodesmia, which shows a high morphologic and genetic diversity that that defies systematization by taxonomic or phylogenetic methods. Here we show that hybridization explains the presence of discordant morphs and that European species are interconnected through cross-mating in a single reproductive network, a syngameon, despite which species remain largely distinct and distinguishable. Whole genome data reflect the important role played by genome defense mechanisms in the genomic stabilization of fungal hybrids. The recurrence of Repeat Induced Point mutations (RIP) shapes genomes with islands of suppressed recombination and loss of gene content, which in turn generates a feedback loop reinforcing the lack of reproductive isolation through the loss of heterokaryon incompatibility and a tendency towards morphological reduction.