Population genomics and epigenomics provide insights into the evolution of facultative asexuality in plants

Abstract Many organisms, particularly plants, can reproduce both sexually and asexually but with varying frequencies. Because variations in the reproductive system profoundly affect fitness and genomic diversity, natural selection should act on changes between sexual and asexual types of propagation. However, the genomic evidence of natural selection driving switches between reproductive systems remains scarce, and the evolutionary consequences of such switches on the genomic and epigenomic diversity remain controversial. Here, by analyzing population genomes and epigenomes of Spirodela polyrhiza (L.) Schleid., a facultatively asexual angiosperm, we show that while the genomic diversity and DNA methylation levels are very low, they vary among populations. These variations are associated with both the demographic history and the frequency of sexual reproduction in each population. A genome-wide scan revealed that multiple genes involved in flowering and embryogenesis were under positive selection, consistent with the hypothesis that natural selection drove the evolution of asexuality in this plant. Together, these results provide new insights into the evolution of plant reproductive systems and suggest that natural selection can drive the evolutionary changes of asexuality, which in turn alters the levels of genomic and epigenomic diversity.