Connecting theory and data to understand recombination rate evolution

Abstract

Meiotic recombination is necessary for successful gametogenesis in most sexually reproducing organisms and is a fundamental genomic parameter, influencing the efficacy of selection and the fate of new mutations. The molecular and evolutionary functions of recombination should impose strong selective constraints on the range of recombination rates. Yet, variation in recombination rate is observed on a variety of genomic and evolutionary scales. In the past decade, empirical studies have described variation in recombination rate within genomes, between individuals, between sexes, between populations and between species. At the same time, theoretical work has provided an increasingly detailed picture of the evolutionary advantages to recombination. Perhaps surprisingly, the causes of natural variation in recombination rate remain poorly understood. We argue that empirical and theoretical approaches to understand the evolution of recombination have proceeded largely independently of each other. Most models that address the evolution of recombination rate were created to explain the evolutionary advantage of recombination rather than quantitative differences in rate among individuals. Conversely, most empirical studies aim to describe variation in recombination rate, rather than to test evolutionary hypotheses. In this Perspective, we argue that efforts to integrate the rich bodies of empirical and theoretical work on recombination rate are crucial to moving this field forward. We provide new directions for the development of theory and the production of data that will jointly close this gap.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

“…A third possibility is that recombination itself is frequently subject to directional selection (Segura et al. ; Dapper and Payseur ; Ritz et al. ), driving divergence at the underlying genes.…”

“…). 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. ).…”

“…Genomic regions ranging in size from short sequences to entire chromosomes vary in recombination rate-both within and between species (Burt and Bell 1987;Broman et al 1998;Jeffreys et al 2005;Coop and Przeworski 2007;Kong et al 2010;Smukowski and Noor 2011;Comeron et al 2012;Segura et al 2013;Dapper and Payseur 2017;Stapley et al 2017). 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 2017;Ritz et al 2017). For example, the form, intensity, and significance of natural selection as a driver of recombination rate evolution are unknown.…”

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).…”