Variation in recombination frequency and distribution across eukaryotes: patterns and processes

Abstract

Recombination, the exchange of DNA between maternal and paternal chromosomes during meiosis, is an essential feature of sexual reproduction in nearly all multicellular organisms. While the role of recombination in the evolution of sex has received theoretical and empirical attention, less is known about how recombination rate itself evolves and what influence this has on evolutionary processes within sexually reproducing organisms. Here, we explore the patterns of, and processes governing recombination in eukaryotes. We summarize patterns of variation, integrating current knowledge with an analysis of linkage map data in 353 organisms. We then discuss proximate and ultimate processes governing recombination rate variation and consider how these influence evolutionary processes. Genome-wide recombination rates (cM/Mb) can vary more than tenfold across eukaryotes, and there is large variation in the distribution of recombination events across closely related taxa, populations and individuals. We discuss how variation in rate and distribution relates to genome architecture, genetic and epigenetic mechanisms, sex, environmental perturbations and variable selective pressures. There has been great progress in determining the molecular mechanisms governing recombination, and with the continued development of new modelling and empirical approaches, there is now also great opportunity to further our understanding of how and why recombination rate varies.This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

Molecular evolution of the meiotic recombination pathway in mammals

“…; Stapley et al. ). The genetic changes responsible for this evolution remain unknown, but they must have occurred in the pathway that regulates the formation of crossovers.…”

“…; Dapper and Payseur ; Stapley et al. ). Despite important insights about the conditions that favor recombination rate evolution from theoretical work, the balance of evolutionary forces responsible for observed patterns of inter‐individual variation in nature has rarely been examined (Dapper and Payseur ; Ritz et al.…”

Karyotypes and recombination patterns of the Common Swift (Apus apus Linnaeus, 1758) and Eurasian Hobby (Falco subbuteo Linnaeus, 1758)

“…For this reason, the number of recombination events (crossovers) per genome (recombination rate) and their distribution along the chromosomes are considered as important genomic characteristics of species and studied actively in plants, fungi and animals (mostly mammals). These studies demonstrated substantial interspecies variation in recombination rate (Dumont and Payseur 2008;Frohlich et al 2015;Dapper and Payseur 2017;Stapley et al 2017) while withinpopulation variation was found to be of the same magnitude across various taxa (Ritz et al 2017). The minimum possible rate of recombination is constrained by the necessity of at least one crossover per pair of homologous chromosomes to ensure their orderly segregation in the first meiotic division.…”

“…Thus, the total genome size and the total length of the synaptonemal complex (SC, the core structure of pachytene chromosomes) may also serve as predictors of species-specific recombination rate (Peterson et al 1994;Kleckner et al 2003). While molecular and cellular mechanisms controlling the recombination rate are more or less clear, the adaptive importance of interspecies differences for this trait remains a matter of discussion (Stapley et al 2017;Dapper and Payseur 2017;Ritz et al 2017).…”

Male Meiotic Recombination in the Steppe Agama, <b><i>Trapelus sanguinolentus</i></b> (Agamidae, Iguania, Reptilia)

“…There are different hypotheses considering the rate of recombination as an adaptive characteristic or associating it with species' phylogeny, ecology, and population structure [Burt and Bell, 1987;Otto and Barton, 1997;Burt, 2000;Barton and Otto, 2005;Butlin, 2005;Segura et al, 2013;Stapley et al, 2017]. According to the theoretical models, elevated recombination rates can be beneficial in unstable or heterogeneous environments and arise in response to high selection pressure, ensuring faster and more efficient adaptation [Otto and Michalakis, 1998;Lenormand and Otto, 2000].…”