A history of both clonality and recombination governs the population structure of Alternaria endophyte communities on prairie Dalea

Abstract

Prairie has become one of the most endangered biomes in North America under changing climates engendered by anthropogenic activity. The patterns of diversity we observe of native prairie species in remnant prairie sites are the outcome of both historical and contemporary processes, and understanding these underlying processes will inform the responses of these populations to future environmental changes. The assembly of fungal endophyte communities within plants depends on the complex interactions of fungal taxa, their host plants, and the abiotic environment. Prairie plant communities provide a unique avenue to explore the interplay of biotic and abiotic factors affecting endophyte communities, since the historical distribution of prairies spans a broad range of temperature and precipitation, while the distances between small fragments of contemporary prairie communities may challenge the dispersal capabilities of these otherwise ubiquitous fungi. We sampled foliar fungal endophytes from two native prairie legumes, purple and white prairie clovers (Dalea purpurea and D. candida), in 17 remnant prairie sites across Minnesota in order to evaluate the relative contributions of abiotic factors, host species, and dispersal limitation to the diversity and structure of these communities. We found that similarity of communities was significantly associated with their location along a temperature and precipitation gradient, and we showed a distance-decay relationship that suggests dispersal limitations only over very large spatial scales. Although the effect of host species was small relative to these other factors, the two Dalea species maintained distinct communities within sites where they co-occur. Our results illustrate the capacity of many of these endophyte taxa to disperse over large distances and across heterogeneous biotic and abiotic environments and suggest that the interplay of biotic and abiotic factors maintains high diversity observed in endophyte communities. Our results showed that community composition of endophytic fungi in Dalea spp. varied along a precipitation and temperature gradient, among hosts, and in apparent response to the abundance of Alternaria spp., but left unexplained patterns of genetic variation among the many isolates assigned to Alternaria alternata. We used genotyping-by-sequencing (GBS) to assess population genetic structure of endophytic Alternaria among sampling sites and between host species, and compare levels of recombination and clonality and assess evidence for sexual or parasexual reproduction in these communities. We found cryptic diversity among sequenced samples, as only a subset aligned well to A. alternata reference genomes. Analysis of sequences closely related to reference A. alternata genomes, treated here as a single species, revealed a high level of clonality, and genotypic diversity shared across populations. However, we also detected evidence of recombination events consistent with sexual or parasexual reproduction, as well as two mating types, MAT1-1 and MAT1-2, which were present in roughly equal frequencies in all but one sampled population. Together, the results suggest recent asexual proliferation after rapid colonization of the sampled sites from an ancestral source population. Recombination likely occurred more frequently in the source population, and is now rare.