Ecological opportunity and the onset of polyploid niche expansion waves

Abstract

Polyploidy, the presence of more than two sets of chromosomes, has evolved many times across the tree of life, yet we still do not know why some polyploid lineages persist while most go extinct. The establishment of polyploid populations is often reported to be associated with harsh environmental conditions, and stress tolerance in particular, which have led to the widespread view that polyploidy-specific niche requirements are key to their persistence at ecological and evolutionary timescales. Here, we reevaluate this perspective through a classical mathematical model of polyploid establishment, for which we provide new analytical and numerical results, along with an empirical case study. We show that simple eco-evolutionary processes at the margins of diploid range-expansion waves, more specifically ecological drift and dispersal limitation, can be sufficient to allow polyploid populations to carve out their own space, without any a priori adaptive advantage over their diploid ancestors. Our modelling effort reveals three key insights. First, polyploids most readily gain a foothold at the low-density front of a diploid range expansion wave, where ecological drift is strongest. Second, limited dispersal accelerates spatial clustering of polyploid organisms through assortative mating. Third, once spatially segregated, diploid and polyploid populations experience different environments, so natural selection can drive niche divergence. We illustrate these interconnected principles by simulating the phylogeographic history of a well-documented autopolyploid complex of Neobatrachus Australian burrowing frogs. Altogether, our results provide a neutral baseline against which the ecological consequences of polyploidization can be readily detected and inferred within natural populations. Significance statementPolyploidy, having multiple copies of the entire set of chromosomes, underpins major innovations in both animals and plants and fuels biodiversity. Yet, why some polyploid lineages are successful while others fail remains unclear. Our study shows that simple eco-evolutionary forces, specifically ecological drift at the edge of an expanding range and limited dispersal, can enable polyploids to establish and become geographically separated from their diploid relatives, even without any inherent adaptive benefits. This spatial segregation then exposes each cytotype to distinct environments, setting the stage for natural selection to operate. Our neutral theoretical framework helps biologists disentangle when polyploidy itself drives adaptation and when success is just a matter of being in the right place at the right time.