Demographic History Inference and the Polyploid Continuum

Abstract

Polyploidy is an important generator of evolutionary novelty across diverse groups in the Tree of Life, including many crops. However, the impact of whole-genome duplication (WGD) depends on the mode of formation: doubling within a single lineage (autopolyploidy) versus doubling after hybridization between two different lineages (allopolyploidy). Researchers have historically treated these two scenarios as completely separate cases based on patterns of chromosome pairing, but these cases represent ideals on a continuum of chromosomal interactions among duplicated genomes. Understanding the history of polyploid species thus demands quantitative inferences of demographic history and rates of exchange between subgenomes. To meet this need, we developed diffusion models for genetic variation in polyploids with subgenomes that cannot be bioinformatically separated and with potentially variable inheritance patterns, implementing them in the dadi software. We validated our models using forward SLiM simulations and found that our inference approach is able to accurately infer evolutionary parameters (timing, bottleneck size) involved with the formation of auto- and allotetraploids, as well as exchange rates in segmental allotetraploids. We then applied our models to empirical data for allotetraploid shepherd's purse (Capsella bursa-pastoris), finding evidence for allelic exchange between the subgenomes. Taken together, our model provides a foundation for demographic modeling in polyploids using diffusion equations, which will help increase our understanding of the impact of demography and selection in polyploid lineages.

Genetic variation in Loudetia simplex supports the presence of ancient grasslands in Madagascar

“…The majority of loci examined were consistent with neutral expectations based on simulations (Table S6), and the proportion of loci with significant Tajima's D statistics were exaggerated when ignoring heterozygosity (Table 1). Although, the estimates of nucleotide diversity and simulations under the standard neutral coalescent used here should be reasonable for polyploids in cases of perfect multisomic inheritance in outcrossers (Arnold et al, 2012; Blischak et al, 2023), we note that the presence of subgenome structure and selfing could cause deviations in expectations of allele frequencies (e.g., Blischak et al, 2023; Meirmans & Van Tienderen, 2013; Ronfort et al, 1998). The mechanism of polyploidization is unknown in L. simplex , but our results do provide some expectations of how genotyping choices for polyploids can impact standard summary statistic estimates.…”

“…Large population genomic studies in plants that can leverage demographic estimates from SFS (e.g., Blischak et al, 2023; Excoffier et al, 2013; Liu & Fu, 2020) are commonly focused on temperate regions (e.g., Yamaura et al, 2019) and species exploited for energy or agriculture (e.g., Huang et al, 2014; Wang et al, 2017). Thus, it is tempting to leverage models that use gene trees as data such as the EBSP (Heled & Drummond, 2008) or other extensions of skyline plots (Pybus et al, 2000), as they could be paired with relatively low‐cost target‐enrichment strategies that yield multi‐locus nuclear data while stretching material quality.…”

“…An array of tools now exists to estimate the effective population size ( N e ) of species through time. As generating genomic data for non‐model groups has become more accessible, population genomic methods that utilize precisely estimated site frequency spectra (SFS; Blischak et al, 2023; Excoffier et al, 2013; Gutenkunst et al, 2009; Liu & Fu, 2020; Nielsen, 2000) have become a valuable tool for reconstructing the demographic history of natural populations. There are still barriers to generating population genomic data though, either due to the lack of suitable tissue, an appropriate reference genome, or costs.…”

Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus

“…This effect is driven by the merger of evolutionarily diverged genomes, which frequently results in remodeling of epigenetic markers (Madlung et al, 2001; Edger et al, 2017; Bird et al, 2021), alterations in gene regulation (Chen, 2007), and activation of transposable elements (Vicient and Casacuberta, 2012). Importantly, there is also a continuum of polyploidy as parental genomes within and among species can vary in evolutionary distance and subsequent genome evolution blurs the distinction between autopolyploidy and allopolyploidy (Stebbins 1947; Leal-Bertioli et al 2018; Mason and Wendel 2020; Blischak et al 2022; Bomblies 2022). Subgenome expression dominance has been defined in terms of a subgenome possessing a greater amount of dominantly expressed homoeologs and has been identified in many allopolyploid species, including maize (Schnable et al 2011) Mimulus peregrinus (Edger et al 2017), garden strawberry (Edger et al 2019), Brassica rapa (Cheng et al 2012; Cheng et al 2016), and a population of resynthesized Brassica napus (Bird et al 2021).…”

“…This effect is driven by the merger of evolutionarily diverged genomes, which frequently results in remodeling of epigenetic markers (Madlung et al, 2001;Edger et al, 2017;Bird et al, 2021), alterations in gene regulation (Chen, 2007), and activation of transposable elements (Vicient and Casacuberta, 2012). Importantly, there is also a continuum of polyploidy as parental genomes within and among species can vary in evolutionary distance and subsequent genome evolution blurs the distinction between autopolyploidy and allopolyploidy (Stebbins 1947;Leal-Bertioli et al 2018;Mason and Wendel 2020;Blischak et al 2022;Bomblies 2022).…”