Demographic History and Natural Selection Shape Patterns of Deleterious Mutation Load and Barriers to Introgression across Populus Genome

Abstract

Hybridization and resulting introgression are important processes shaping the tree of life and appear to be far more common than previously thought. However, how the genome evolution was shaped by various genetic and evolutionary forces after hybridization remains unresolved. Here we used whole genome resequencing data of 227 individuals from multiple widespread Populus species to characterize their contemporary patterns of hybridization and to quantify genomic signatures of past introgression. We observe a high frequency of contemporary hybridization and confirm that multiple previously ambiguous species are in fact F1 hybrids. Seven species were identified, which experienced different demographic histories that resulted in strikingly varied efficacy of selection and burdens of deleterious mutations. Frequent past introgression has been found to be a pervasive feature throughout the speciation of these Populus species. The retained introgressed regions, more generally, tend to contain reduced genetic load and to be located in regions of high recombination. We also find that in pairs of species with substantial differences in effective population size, introgressed regions are inferred to have undergone selective sweeps at greater than expected frequencies in the species with lower effective population size, suggesting that introgression likely have higher potential to provide beneficial variation for species with small populations. Our results, therefore, illustrate that demography and recombination have interplayed with both positive and negative selection in determining the genomic evolution after hybridization.

The western redcedar genome reveals low genetic diversity in a self-compatible conifer

“…We estimated π to be 0.0027 in SCOs and 0.0020 across all sequenced space. These estimates are lower than many other plant species using comparable methods, for example, Norway spruce (π = 0.0049–0.0063) ( Wang et al 2020 ), weedy broomcorn millet (π = 0.14; Panicum miliaceum ) ( Li et al 2021 ), and most Populus species (π = 0.0041–0.011) ( Liu et al 2022 ). We found lower π estimates only in highly cultivated plants, such as soybean (π = 0.0015; Glycine spp.)…”

“…We found lower π estimates only in highly cultivated plants, such as soybean (π = 0.0015; Glycine spp.) ( Bayer et al 2022 ), or rare, isolated species, such as Populus qiongdaoensis (π = 0.0014), which is restricted to a single small island and has an estimated N e of about 500 ( Liu et al 2022 ). Additionally, our probe selection strategy for genotyping targeted regions of high variability owing to the very low levels of polymorphism in initial sequencing runs.…”

The western redcedar genome reveals low genetic diversity in a self-compatible conifer

“…We found lower π estimates only in highly cultivated plants, such as soybean (π = 0.0015; Glycine spp.) (Bayer et al 2022), or rare, isolated species, such as Populus qiongdaoensis (π = 0.0014), which is restricted to a single small island and has an estimated N e of ∼500 (Liu et al 2022). Additionally, our probe selection strategy for genotyping targeted regions of high variability due to the very low levels of polymorphism in initial sequencing runs.…”

Repeated out-of-Africa expansions of Helicobacter pylori driven by replacement of deleterious mutations

“…Deleterious mutations have been shown to be important during hybridization in several eukaryotic systems, including swordfish 26 , trees 27 and Neanderthal introgression into modern humans 25 . In these systems, recombination rate variation has been shown to be crucial in determining the rate of introgression that has taken place in different regions of the genomes.…”

“…Third we show that ancestry from these invading lineages is higher in regions of the genome where nonsynonymous mutations are segregating within the bottlenecked populations, implying that selection has acted to purge these mutations during admixture. Deleterious mutations have been shown to be important during hybridization in several eukaryotic systems, including swordfish 26 , trees 27 and Neanderthal introgression into modern humans 25 . In these systems, recombination rate variation has been shown to be crucial in determining the rate of introgression that has taken place in different regions of the genomes.…”