The genetic consequences of range expansion and its influence on diploidization in polyploids

Abstract

Despite newly formed polyploids being subjected to myriad fitness consequences, the relative prevalence of polyploidy both contemporarily and in ancestral branches of the tree of life suggests alternative advantages that outweigh these consequences. One proposed advantage is that polyploids have an elevated adaptive potential that enables them to colonize novel habitats such as previously glaciated areas. However, previous research conducted in diploids suggests that range expansion comes with a fitness cost as deleterious mutations may fix rapidly on the expansion front. Here, we interrogate the potential consequences of expansion in polyploids by conducting spatially explicit forward-in-time simulations of autopolyploids, allopolyploids, and diploids to investigate how ploidy and inheritance patterns impact the relative ability of polyploids to expand their range. We show that under realistic dominance models, autopolyploids suffer greater fitness reductions than diploids as a result of range expansion due to the fixation of increased mutational load that is masked in the range core. Alternatively, the disomic inheritance of allopolyploids provides a shield to this fixation resulting in minimal fitness consequences under an empirically estimated DFE. In light of this advantage provided by disomy, we investigate how range expansion may influence cytogenetic diploidization through the reversion to disomy in autotetraploids. We show that under both a model of where the mode of inheritance is determined by a small number of loci and a model where inheritance is regulated by chromosomal similarity, disomy evolves more rapidly on the expansion front than in the range core, and that this dynamic inheritance model has additional effects on fitness. Together our results point to a complex interaction between dominance, ploidy, inheritance, and recombination on fitness as a population spreads across a geographic range.