Interspecific transfer of genetic information through polyploid bridges

Abstract

Hybridization blurs species boundaries and leads to intertwined lineages resulting in reticulate evolution. Polyploidy, the outcome of whole genome duplication (WGD), has more recently been implicated in promoting and facilitating hybridization between polyploid species, potentially leading to adaptive introgression. However, because polyploid lineages are usually ephemeral states in the evolutionary history of life it is unclear whether WGD-potentiated hybridization has any appreciable effect on their diploid counterparts. Here, we develop a model of cytotype dynamics within mixed-ploidy populations to demonstrate that polyploidy can in fact serve as a bridge for gene flow between diploid lineages, where introgression is fully or partially hampered by the species barrier. Polyploid bridges emerge in the presence of triploid organisms, which despite critically low levels of fitness, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents polyploid-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, allowing a more efficient sorting of alleles at higher-ploidy levels before introgression into diploid gene pools. Additionally, we derive an analytical approximation for the rate of gene flow at the tetraploid level necessary to supersede introgression between diploids with nonzero introgression rates, which is especially relevant for plant species complexes, where interspecific gene flow is ubiquitous. Altogether, our results illustrate the potential impact of polyploid bridges on the (re)distribution of genetic material across ecological communities during evolution, representing a potential force behind reticulation. SIGNIFICANCE : Polyploidy, which results from the duplication of an organism’s entire genome, is a known source of genetic novelty that promotes speciation, thus contributing to the evolution and distribution of biodiversity. Its ecoevolutionary interactions with coexisting diploid relatives are nonetheless elusive. Here, we have developed a theoretical model to understand the temporal dynamics of mixed-ploidy populations, revealing that polyploidy may serve as a bridge for gene flow across diploid species boundaries. Due to exceptional hybridization potential and the intricate mating dynamics specific to mixed-ploidy populations, polyploids may play an important role in the emergence of intertwined lineages. Our findings provide, therefore, insights into the mechanisms that underlie the distribution of genetic material within ecosystems, leading to reticulate evolutionary histories.