Allopolyploid Speciation Accompanied by Gene Flow in a Tree Fern

Hybridization in plants may result in hybrid speciation or introgression and, thus, is now widely understood to be an important mechanism of species diversity on an evolutionary timescale. Hybridization is particularly common in ferns, as is polyploidy, which often results from hybrid crosses. Nevertheless, hybrid speciation as an evolutionary process in fern lineages remains poorly understood. Here, we employ flow cytometry, phylogeny, genomewide single nucleotide polymorphism data sets, and admixture and coalescent modeling to show that the scaly tree fern, Gymnosphaera metteniana is a naturally occurring allotetraploid species derived from hybridization between the diploids, G. denticulata and G. gigantea. Moreover, we detected ongoing gene flow between the hybrid species and its progenitors, and we found that G. gigantea and G. metteniana inhabit distinct niches, whereas climatic niches of G. denticulata and G. metteniana largely overlap. Taken together, these results suggest that either some degree of intrinsic genetic isolation between the hybrid species and its parental progenitors or ecological isolation over short distances may be playing an important role in the evolution of reproductive barriers. Historical climate change may have facilitated the origin of G. metteniana, with the timing of hybridization coinciding with a period of intensification of the East Asian monsoon during the Pliocene and Pleistocene periods in southern China. Our study of allotetraploid G. metteniana represents the first genomic-level documentation of hybrid speciation in scaly tree ferns and, thus, provides a new perspective on evolution in the lineage.