Chromosome size affects sequence divergence between species through the interplay of recombination and selection

Abstract

The structure of the genome shapes the distribution of genetic diversity and sequence divergence. To investigate how the relationship between chromosome size and recombination rate affects sequence divergence between species, we combined empirical analyses and evolutionary simulations. We estimated pairwise sequence divergence among 15 species from three different mammalian clades-Peromyscus rodents, Mus mice, and great apes-from chromosome-level genome assemblies. We found a strong significant negative correlation between chromosome size and sequence divergence in all species comparisons within the Peromyscus and great apes clades but not the Mus clade, suggesting that the dramatic chromosomal rearrangements among Mus species may have masked the ancestral genomic landscape of divergence in many comparisons. Our evolutionary simulations showed that the main factor determining differences in divergence among chromosomes of different sizes is the interplay of recombination rate and selection, with greater variation in larger populations than in smaller ones. In ancestral populations, shorter chromosomes harbor greater nucleotide diversity. As ancestral populations diverge, diversity present at the onset of the split contributes to greater sequence divergence in shorter chromosomes among daughter species. The combination of empirical data and evolutionary simulations revealed that chromosomal rearrangements, demography, and divergence times may also affect the relationship between chromosome size and divergence, thus deepening our understanding of the role of genome structure in the evolution of species divergence.

Genomic architecture drives population structuring in Amazonian birds

“…This process should lead to an overall higher recombination rate in shorter chromosomes (Manthey et al 2021; Farré et al 2012; Kawakami et al 2014; Haenel et al 2018; Kaback et al 1992). Similar results to the one we obtained for L. vociferans have also been observed in other species of birds and mammals (Dutoit et al 2017a; Pessia et al 2012; Kartje et al 2020) and could be explained by a reduced synteny between our reference and the zebra finch genome, or the historical demography of the species, which in some cases can reverse the expected associations between recombination, genetic diversity, and chromosome size (Tigano et al 2021; Van Belleghem et al 2018). However, the former scenario was less likely due to the relative stability of chromosomes across avian species (Ellegren 2010).…”

“…Genomic architecture was likely conserved over the timeframe of our study, indicating that a stable genomic landscape might shape the demographic and phylogenetic histories of closely related populations in similar ways (Vijay et al 2017; Van Doren et al 2017; Dutoit et al 2017b; Delmore et al 2018; Tigano et al 2021). For example, consistent variation in Fst values across the genomes of population pairs of the same species were likely reflecting the genomic landscape of the ancestral population.…”

“…recombination and selection) and extrinsic (e.g., gene flow) genomic processes lead to phylogenetic conflict affecting genome-wide estimates. In the presence of gene flow, low recombination areas are more prone to maintain the ancient branching signal (Li et al 2019; Tigano et al 2021). The strong linkage in low recombination regions should lead to the more effective removal of alleles introduced by hybridization that are more likely to be deleterious (Nachman and Payseur 2012; Schumer et al 2018).…”

“…Although recent studies show that linked selection impacts a larger proportion of the genome than previously thought (Pouyet et al 2018;Kern and Hahn 2018), the degree of this impact varies between species (Tigano et al 2021;Jensen et al 2019). For instance, the divergence between populations with high rates of gene flow might be restricted to small areas of the genome, maintained by strong divergent selection whereas the vast majority of the genome might show reduced differentiation due to widespread introgression (Ellegren et al 2012).…”

“…On the other hand, demographic parameters may be heavily biased when recombination and selection are neglected (Pouyet et al 2018;Ewing and Jensen 2016). This conundrum indicates that methods designed to simultaneously account for multiple genomic processes, such as recombination, selection, drift, and mutation (Barroso and Dutheil 2021;Johri et al 2020Johri et al , 2021, associated with simulation studies (Tigano et al 2021) might be necessary to unbiasedly obtain evolutionary parameters from genome-wide variation.…”