Population genomics of heterosporous lycophytes: allopatric speciation and historical persistence through paleoclimatic fluctuations

SUMMARY

Speciation is the fundamental process driving the origin of earth biodiversity. While speciation mechanisms have been revealed in many plant taxa, the evolutionary dynamics of heterosporous lycophytes remain largely unexplored. Here, we used the Selaginella sanguinolenta group, comprising seven montane species in eastern Asia, as a model system. We generated a high‐quality, chromosome‐level reference genome for S . aitchisonii , conducted whole‐genome resequencing of 191 individuals across 49 populations, and integrated population genomic, phylogenomic, morphological, and ecological analyses. Our results revealed that strong geographic isolation, driven by Miocene paleogeographic events, led to high genetic differentiation and restricted interspecific gene flow. The unique combination of heterospory and independent gametophyte generations might exacerbate extreme inbreeding, further impeding the ability of these lineages to surmount geographical barriers. Ecological niche divergence indicated that these species experience heterogeneous selection pressures; moreover, evidence of selective sweeps, leaf arrangement variation, and functional gene divergence indicates that natural selection gives rise to new species with environmentally adaptive traits. Demographic reconstructions revealed a shared trajectory of expansion followed by contraction into bottlenecks from the late Miocene to the Pliocene. Montane refugia likely played a role in species persistence, preserving genetic diversity for the postglacial expansions observed in four species since the Last Interglacial. We conclude that the S. sanguinolenta group underwent allopatric speciation since the Miocene and successfully persisted through severe Quaternary climatic fluctuations, which provides novel insights based on population genomic analysis into the evolution of early‐diverging vascular plants.