Neutral processes underlying the macro eco-evolutionary dynamics of mixed-ploidy systems

Abstract

Polyploidy, i.e. the occurrence of multiple sets of chromosomes, is regarded as an important phenomenon in plant ecology and evolution, with all flowering plants likely having a polyploid ancestry. Owing to genome shock, minority cytotype exclusion and reduced fertility, polyploids emerging in diploid populations are expected to face significant challenges to successful establishment. Their establishment and persistence are often explained by possible fitness or niche differences that would relieve the competitive pressure with diploid progenitors. Experimental evidence for such advantages is, however, not unambiguous, and considerable niche overlap exists among most polyploid species and their diploid counterparts. Here, we develop a neutral spatially explicit eco-evolutionary model to understand whether neutral processes can explain the eco-evolutionary patterns of polyploids. We present a general mechanism for polyploid establishment by showing that sexually reproducing organisms assemble in space in an iterative manner, reducing frequency-dependent mating disadvantages and overcoming potential reduced fertility issues. Moreover, we construct a mechanistic theoretical framework that allows us to understand the long-term evolution of mixed-ploidy populations and show that our model is remarkably consistent with recent phylogenomic estimates of species extinctions in the Brassicaceae family.

Dynamics of mixed-ploidy populations under demographic and environmental stochasticities

“…Also, group-based associative mating, as de-fined by mating choice, allows the rate of intra-cytotype gamete exchange to be defined without explicitly defining pollinator transitions, spatial distance, or other demographic factors. Previous spatially explicit theoretical work suggests the probability of establishment of a polyploid is influenced by three factors; local majority status (Baack 2005;Griswold 2021;Kauai et al 2023;Spoelhof et al 2020), pollen and seed dispersal probability distribution shape (Van Drunen and Friedman 2022), and clonal ability (Levin 2021;Spoelhof et al 2020;Van Drunen and Friedman 2022). Of these, our model can incorporate the first two via our mating choice parameter.…”

“…Microgeographic organization in naturally occurring populations of mixed cytoypes has rarely been investigated; however, theoretical models have repeatedly suggested that spatial segregation is essential for neoautotetraploid persistence (Baack 2005;Griswold 2021;Kauai et al 2023;Spoelhof et al 2020;Van Drunen and Friedman 2022). Despite the theoretical expectation of spatial divergence, mixed cytotype populations lacking spatial segregation have been observed in many taxa (as reviewed by Kolář et al 2017).…”

Interspecific transfer of genetic information through polyploid bridges

“…Ongoing efforts to recover WGDs in the history of life (7, 8) reveal that several of such events seem to cluster around periods of environmental upheaval (9-11), such as the mass extinction event at the Cretaceous-Paleogene (K-Pg) boundary (12, 13), indicating a potential enhanced capacity of polyploids to adapt and respond to stressful conditions (4, 14-17). Notwithstanding the presumed adaptive potential, phylogenetic and theoretical analyses also suggest that polyploid lineages display greater extinction rates than diploids (18-20), or eventually evolve to the more stable diploid state through the process of rediploidization (11). Despite the ambivalence, WGD is widely recognized to have important implications for the generation of genetic novelty over macroevolutionary scales (3, 9, 21-23).…”

“…The current understanding of the mechanisms underlying the emergence and dynamics of polyploidy within diploid populations stems from extensive theoretical and experimental research, which continue to provide valuable insights on the frequency and occurrence of WGD in nature (14, 20, 48-53) . Most models assume that polyploids primarily emerge by the union of unreduced (diploid) gametes, which are formed by a rare event resulting from the non-segregation of chromosomes during meiosis (39, 54, 55).…”

Doubling down on polyploidy

“…Publications from just the past year show active interest in polyploid diversity, establishment, and persistence (e.g. Carta & Escudero, 2023; Kauai et al ., 2023).…”