Moving beyond assumptions: Polyploidy and environmental effects explain a geographical parthenogenesis scenario in European plants

Abstract

Geographical parthenogenesis (GP) describes the phenomenon that apomicts tend to have larger distribution areas and/or occur at higher altitudes or latitudes compared to sexual relatives. However, the complex effects of genome-wide heterozygosity, ploidy, reproduction mode (sexual vs. apomictic), and environment shaping GP of plants are still not well understood. We ascertained ploidy and reproduction mode by flow cytometry of 221 populations, and added genomic RADseq data (maximum 33,165 loci) of 80 taxa of the Ranunculus auricomus polyploid plant complex in temperate Europe. We observed 7% mainly diploid sexual, 28% facultative apomictic (mean sexuality 7.1%), and 65% obligate apomictic populations. Sexuals occupied a more southern, smaller distribution area, whereas apomicts expanded their range to higher latitudes. Within the complex, we detected three main genetic clusters and highly reticulate relationships. A genetically-informed path analysis using GLMMs revealed several significant relationships. Sexuality of populations (percent of sexual seeds) was higher in diploids compared to polyploids, associated with more petals, and similar between forests and open habitats. In contrast to other apomictic plant complexes, sexuality was mainly positively correlated to solar radiation and isothermality, which fits the southern distribution. We found up to three times higher heterozygosity in polyploids compared to diploids, and generally more heterozygous individuals in forests compared with open habitats. Interestingly, we revealed a previously unknown positive association between heterozygosity and temperature seasonality, suggesting a higher resistance of polyploids to more extreme climatic conditions. We provide empirical evidence for intrinsic and extrinsic factors shaping the GP pattern in a polyploid plant complex.