Population genomics of the gametophyte-only fern Vittaria appalachiana provides insights into clonal plant evolution.

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How asexually reproducing organisms maintain genetic diversity and adaptive potential is a long-standing question in evolutionary biology. Asexual lineages have historically been thought of as evolutionary dead ends, yet some exhibit remarkable persistence through time. The gametophyte-only fern Vittaria appalachiana is a clonal eukaryote, the focus of extensive study due to its peculiar habit and life history, and is an excellent system to explore the consequences of asexuality. Using reduced representation sequencing and life cycle simulations, we assess theoretical expectations for genomic consequences of long-term asexual reproduction and test hypotheses about its origin and demographic history. We show that V. appalachiana colonies are not patches of single genotypes but are mosaics of genetic diversity, and the accumulation of mutations in the absence of recombination plays an important role in driving this diversity. We identify increased genomic variation, excess heterozygosity, decreased population differentiation, and increased effective population size, all of which are consistent with the expectations for prolonged clonality. Our analyses support the hypothesis that the loss of sexual reproduction in V. appalachiana occurred during the Last Glacial Maximum. Our results from empirical and simulation-based analyses illuminate how an asexual eukaryote generates, retains, and partitions genomic diversity.