Maintenance of Fungal Pathogen Species That Are Specialized to Different Hosts: Allopatric Divergence and Introgression through Secondary Contact

Abstract

Sympatry of species that lack complete prezygotic isolation is ideal for the study of how species can be maintained in the face of potential gene flow. This is particularly important in the context of emerging diseases on new hosts because pathogen adaptation is facilitated by reduced gene flow from ancestral populations. Here, we investigated divergence and gene flow between two closely related fungal species, Microbotryum lychnidis-dioicae and M. silenes-dioicae, causing anther-smut disease on the wide-spread plant species Silene latifolia and S. dioica, respectively. Using model-based clustering algorithms on microsatellite data from samples across Europe, we identified rare disease transmission between the host species and rare pathogen hybrids. Using a coalescent-based approach and an isolation-with-migration model, the age of divergence between the two fungal species was estimated at approximately 4.2 × 10(5) years. Levels of gene flow were low and concentrated in very recent times. In addition, gene flow appeared unidirectional from M. silenes-dioicae to M. lychnidis-dioicae. Altogether, our findings are consistent with a scenario of recurrent introgressive hybridization but at a very low level and through secondary contact following initial divergence in allopatry. Asymmetry in the direction of gene flow mirrors previous findings on introgression between the two host plants. Our study highlights the consequences of bringing closely related pathogens into contact, which is increasing through modern global changes and favors cross-species disease transmission, hybridization, and introgression by pathogens.

Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism

“…Trans-specific polymorphism in the genealogies of genes in the black stratum never extended to M. lagerheimii, consistent with the lack of linkage between the PR and HD mating-type loci in this species. When calibrated by the previous estimate for the date of the speciation event between M. lychnidis-dioicae and M. silenes-dioicae to 420,000 years ago (38), the divergence between a 1 -and a 2-associated alleles in the black region led to an estimate for the date of linkage between the HD and PR loci of about 1.3 million years ago (95% confidence interval between 1.1 and 1.6 million years) (SI Appendix, SI Text and Table S1). …”

The tempo and modes of evolution of reproductive isolation in fungi

“…Surprisingly, however, the degree of syngamy compatibility did not continue to decrease at larger genetic distances, remaining quite high. That inhibition of interspecific gamete fusion does not further decrease at higher genetic distance is intriguing given the evolution of postsyngamy isolation, with continual increase of hybrid inviability and sterility at these genetic distances, and the overlapping ranges of the species (Bucheli et al, 2000;Le Gac et al, 2007a, b;Hood et al, 2010;Gladieux et al, 2010b;Vercken et al, 2010). One may think that reinforcement would have kept on occurring to avoid producing unfit hybrids, especially at the greatest genetic distances where postsyngamy isolation is the strongest.…”

“…The explanation for the persistence of high degree of syngamy compatibility at large genetic distance may instead be that the strength of selection for increasing assortative mating via mate choice may be too low in Microbotryum, because hybridization is sufficiently rare in nature. The cumulative effects of other presyngamy barriers, such as differences in habitat and pollinator of the plant Evolution of reproductive isolation in fungi T Giraud and S Gourbière species (Goulson and Jerrim, 1997;van Putten et al, 2007;Gladieux et al, 2010b) and high rates of selfing (40.90;Giraud et al, 2005Giraud et al, , 2008bHood and Antonovics, 2000;Gladieux et al, 2010b), may be strong enough such that very few hybrids are produced in nature even with weak preference for conspecifics (Bucheli et al, 2000;Refrégier et al, 2010;Gladieux et al, 2010b;Gibson et al, 2012).…”

The evolution of species concepts and species recognition criteria in plant pathogenic fungi

“…As in other fungal species, the Biological Species Criterion was less discriminating (Le Gac et al 2007b), with little evidence of assortative mating in the form of conjugation initiation in vitro, although hybrid inviability and sterility was observed between the cryptic species (Le Gac et al 2007b;de Vienne et al 2009a). Cross-inoculation studies also appeared less discriminating in vitro than host specificity seen in the field (de Vienne et al 2009b;Gladieux et al 2011). The studies highlight the value of Genealogical Concordance Phylogenetic Species Recognition to validate Phylogenetic Species Criterion and Morphological Species Criterion that have practical application in the field of plant pathology.…”