The origins and adaptive consequences of polyploidy in a dominant prairie grass

Polyploidy is ubiquitous across North American prairies, which provide essential ecosystem services and rich soil for agriculture. Yet the mechanism driving polyploid abundance is unclear. Multiple hypotheses have been proposed including polyploid abundance is proportional to the opportunity for whole genome duplication (WGD), and WGD alters phenotypes that may increase fitness. We tested these two hypotheses together in the mixed-ploidy species Andropogon gerardi, a dominant grass species in endangered North American tallgrass prairies. Leveraging a novel, phased allopolyploid reference genome, we found the A. gerardi hexaploid arose after the C4 grassland expansion in the early Pleistocene, when glacial cycles likely increased secondary contact between the diploid progenitors. We sequenced A. gerardi from 25 popula-tions and examined cytotype performance and morphology in a controlled environment to investigate the consequences of the contemporary mixed-ploidy populations. We found the 9x A. gerardi cytotype is a neopolyploid and a result of recurrent WGD events. Further, we demonstrate the 9x neopolyploids have greater growth and a decreased stomatal pore index, which is adaptive in xeric climates where the 9x cy-totype is most common. Together, our results support both hypotheses for polyploid abundance in North America: WGD is a product of opportunity and can have immediate fitness consequences. Although the changes to fitness may provide an advantage to 9x A. gerardi, the establishment of 9x may lower overall population fitness due to the lower reproductive viability of 9x individuals. Significance statementPolyploid species are abundant in North American prairies and make up many of the dominant species in the ecosystem. This prominence could be a result of whole genome duplication conferring an advantage that increases the frequency of polyploids or could simply indicate that the opportunity for whole genome duplication is higher in this ecosystem, or both. Through examining three polyploidization events in A. gerardi, the dominant species in endangered tallgrass North American prairies, we found whole genome duplication is both surprisingly common and confers traits that are beneficial in some environments.