Per-Nucleus Crossover Covariation and Implications for Evolution

Abstract

Graphical Abstract Highlights d Crossover number is correlated across chromosomes within individual meiotic nuclei d CO covariation results from covariation of chromosome axis lengths within nuclei d CO covariation increases the frequencies of gametes with either many or few COs d Hyper-and hypo-CO gametes aid adaptation in a sporadically fluctuating environment SUMMARY Crossing over is a nearly universal feature of sexual reproduction. Here, analysis of crossover numbers on a per-chromosome and per-nucleus basis reveals a fundamental, evolutionarily conserved feature of meiosis: within individual nuclei, crossover frequencies covary across different chromosomes. This effect results from per-nucleus covariation of chromosome axis lengths. Crossovers can promote evolutionary adaptation. However, the benefit of creating favorable new allelic combinations must outweigh the cost of disrupting existing favorable combinations. Covariation concomitantly increases the frequencies of gametes with especially high, or especially low, numbers of crossovers, and thus might concomitantly enhance the benefits of crossing over while reducing its costs. A four-locus population genetic model suggests that such an effect can pertain in situations where the environment fluctuates: hyper-crossover gametes are advantageous when the environment changes while hypo-crossover gametes are advantageous in periods of environmental stasis. These findings reveal a new feature of the basic meiotic program and suggest a possible adaptive advantage.

Recombination and selection against introgressed DNA

“…These moments can be estimated computationally given sufficient information about the recombination process in males and females. Note, however, that higher moments will depend on meiotic features such as crossover interference along chromosomes and crossover covariation across chromosomes (Wang et al 2019;see Discussion). To estimate higher moments from the recombination process taking into account these meiotic features, one could use simulations of the beam-film model, a physical model of recombination that can be computationally calibrated to accurately reproduce crossover distributions (White et al 2017).…”

“…Recombination rates between adjacent loci are sex-specific, and are interpolated from the linkage maps mentioned above. We assume no crossover interference along chromosomes, and we further assume no crossover covariation across chromosomes (Wang et al 2019). The population size in our simulations is N = 10 5 .…”

“…Crossover covariation. It has recently been shown across diverse eukaryotes that the number of crossovers per chromosome covaries positively across chromosomes within individual meiotic nuclei (Wang et al 2019). This 'crossover covariation' increases the variance of the number of crossovers per gamete, which obviously will affect the distribution of genetic relatedness among relatives.…”

Crossover Interference, Crossover Maturation, and Human Aneuploidy

“…[35,36] The axes of homologs first become coaligned at a distance along their lengths and then become intimately synapsed at ≈100 nm distance via the formation of the synaptonemal complex (SC). 1) The frequency of recombination initiation events is proportional to physical chromosome length, with axis length determining initiation frequency rather than the reverse (discussion in Wang et al [38] ). [35][36][37] Axis association of recombination complexes also has the consequence that the distance metric for recombination is the physical distance along a prophase chromosome, both for initiation and for CO interference.…”

“…Segregation of homologs to opposite poles requires both: [38,76] i) the presence of a chiasma between homologs, which in turn requires both CO(s) and arm cohesion, and ii) co-orientation of sister kinetochores, which is mediated by cohesion in centromeric regions. However, one prominent candidate is sister chromatid arm cohesion.…”