Apomixis goes a long way: Genetic evidence of persistence and long-distance seed dispersal in an ancient landscape

Abstract

Aim: Apomixis is a widespread trait in extreme environments worldwide, yet phylogeographical studies for species exhibiting these complex reproductive systems are still limited to temperate zones in the Northern Hemisphere. Through analyses of a combination of adult plants and seedlings, and nuclear and chloroplast DNA, we assessed the contemporary genetic outcomes of apomixis and phylogeographical patterns in an arid unglaciated landscape to understand the evolutionary trajectory of apomictic species. Location: Pilbara bioregion, north-western Australia. Taxon: Senna glutinosa subsp. glutinosa. Materials and Methods: Spatial patterns of genetic diversity and differentiation in three chloroplast regions and 17 nuclear microsatellite markers were evaluated in 480 plants from 20 populations of S. glutinosa subsp. glutinosa across the Pilbara bioregion. We also germinated and genotyped seed for a progeny analysis to quantify polyembryony and the relative frequency of asexual versus sexual reproduction. Results: We found frequent polyembryony and a high proportion of asexual offspring (84.56%), resulting in low within-population genotypic diversity. The nuclear dataset identified 72 multilocus lineages (MLLs) with moderate pairwise population genetic fixation and low differentiation among populations with no geographically structured genetic clustering. Chloroplast DNA showed high haplotype diversity and a widespread distribution of haplotypes. Only one peripheral population presented a single unique haplotype and MLL. Main Conclusions: Analysis of this woody perennial in an arid landscape shows the influence of apomixis on genetic patterns and species persistence. Haplotype diversity was indicative of long-term persistence within the ancient Pilbara region. Widespread distribution of haplotypes and sharing of several nuclear MLLs among distant populations indicated extensive seed dispersal throughout the study area. The combination of polyploidy, facultative apomixis and extensive seed dispersal maintains genetic variability within local populations and promotes the spread of advantageous genotypes across wide geographical distances. Therefore, apomixis, rather than an evolutionary ‘dead-end’, can be regarded as a mechanism facilitating evolutionary success of apomictic species in extreme and complex environments.