Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

Abstract

Understanding the distribution of crossovers along chromosomes is crucial to evolutionary genomics because the crossover rate determines how strongly a genome region is influenced by natural selection on linked sites. Nevertheless, generalities in the chromosome-scale distribution of crossovers have not been investigated formally. We fill this gap by synthesizing joint information on genetic and physical maps across 62 animal, plant and fungal species. Our quantitative analysis reveals a strong and taxonomically widespread reduction of the crossover rate in the centre of chromosomes relative to their peripheries. We demonstrate that this pattern is poorly explained by the position of the centromere, but find that the magnitude of the relative reduction in the crossover rate in chromosome centres increases with chromosome length. That is, long chromosomes often display a dramatically low crossover rate in their centre, whereas short chromosomes exhibit a relatively homogeneous crossover rate. This observation is compatible with a model in which crossover is initiated from the chromosome tips, an idea with preliminary support from mechanistic investigations of meiotic recombination. Consequently, we show that organisms achieve a higher genome-wide crossover rate by evolving smaller chromosomes. Summarizing theory and providing empirical examples, we finally highlight that taxonomically widespread and systematic heterogeneity in crossover rate along chromosomes generates predictable broad-scale trends in genetic diversity and population differentiation by modifying the impact of natural selection among regions within a genome. We conclude by emphasizing that chromosome-scale heterogeneity in crossover rate should urgently be incorporated into analytical tools in evolutionary genomics, and in the interpretation of resulting patterns.

A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha

“…Recombination rates were greater in the middle of the chromosome arms in M. polymorpha, whereas they were more evenly distributed in P. patens. Therefore, the recombination landscape of the M. polymorpha genome at the large scale is similar to that observed in most flowering plants and the evenly distributed recombination rates seem to be a unique feature of P. patens (Heslop-Harrison, 2000;M ezard et al, 2007;Haenel et al, 2018). Similarly, we found that GC content was significantly higher in the middle of the chromosome arms in M. polymorpha, while it was evenly distributed in the P. patens genome.…”

Genome of an iconic Australian bird: High‐quality assembly and linkage map of the superb fairy‐wren (Malurus cyaneus)

“…In the between‐chromosome comparison, we found that smaller chromosomes tend to have much higher recombination rate and also tend to have much higher gene density (Axelsson, Webster, Smith, Burt, & Ellegren, ). Furthermore, recombination tends to be higher closer to the ends of chromosomes (Haenel, Laurentino, Roesti, & Berner, ). While we can only scratch the surface of these comparisons here, understanding the causes and consequences of recombination rate variation is critical in understanding how genome organization influences variation in the efficiency of selection across the genome.…”

Predictable genome-wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish

“…conclusions about parallelism at the genomic level (Berner and Roesti 2017;Lowry et al 2017;Haenel et al 2018; for exceptions, see Martin et al 2013;Lamichhaney et al 2016;Reid et al 2016;Yeaman et al 2016;Elgvin et al 2017). Second, has the greater ecological difference of the acidic than basic lakes from the ancestral habitat caused asymmetry in the selection of adaptive genetic variation?…”