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

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          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’.

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          Most cited references 177

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          The genomic basis of adaptive evolution in threespine sticklebacks

          Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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            High-resolution mapping of meiotic crossovers and non-crossovers in yeast.

            Meiotic recombination has a central role in the evolution of sexually reproducing organisms. The two recombination outcomes, crossover and non-crossover, increase genetic diversity, but have the potential to homogenize alleles by gene conversion. Whereas crossover rates vary considerably across the genome, non-crossovers and gene conversions have only been identified in a handful of loci. To examine recombination genome wide and at high spatial resolution, we generated maps of crossovers, crossover-associated gene conversion and non-crossover gene conversion using dense genetic marker data collected from all four products of fifty-six yeast (Saccharomyces cerevisiae) meioses. Our maps reveal differences in the distributions of crossovers and non-crossovers, showing more regions where either crossovers or non-crossovers are favoured than expected by chance. Furthermore, we detect evidence for interference between crossovers and non-crossovers, a phenomenon previously only known to occur between crossovers. Up to 1% of the genome of each meiotic product is subject to gene conversion in a single meiosis, with detectable bias towards GC nucleotides. To our knowledge the maps represent the first high-resolution, genome-wide characterization of the multiple outcomes of recombination in any organism. In addition, because non-crossover hotspots create holes of reduced linkage within haplotype blocks, our results stress the need to incorporate non-crossovers into genetic linkage analysis.
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              The genomics of speciation-with-gene-flow.

              The emerging field of speciation genomics is advancing our understanding of the evolution of reproductive isolation from the individual gene to a whole-genome perspective. In this new view it is important to understand the conditions under which 'divergence hitchhiking' associated with the physical linkage of gene regions, versus 'genome hitchhiking' associated with reductions in genome-wide rates of gene flow caused by selection, can enhance speciation-with-gene-flow. We describe here a theory predicting four phases of speciation, defined by changes in the relative effectiveness of divergence and genome hitchhiking, and review empirical data in light of the theory. We outline future directions, emphasizing the need to couple next-generation sequencing with selection, transplant, functional genomics, and mapping studies. This will permit a natural history of speciation genomics that will help to elucidate the factors responsible for population divergence and the roles that genome structure and different forms of hitchhiking play in facilitating the genesis of new biodiversity. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos. Trans. R. Soc. Lond., B, Biol. Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                19 December 2017
                6 November 2017
                6 November 2017
                : 372
                : 1736 , Theme issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’ compiled and edited by Jessica Stapley, Philine G. D. Feulner, Susan E. Johnston, Anna W. Santure and Carole M. Smadja
                Affiliations
                [1 ]Centre for Adaptation to a Changing Environment, IBZ, ETH Zürich , 8092 Zürich, Switzerland
                [2 ]Department of Fish Ecology and Evolution, Centre of Ecology, Evolution and Biogeochemistry, EAWAG Swiss Federal Institute of Aquatic Science and Technology , 6047 Kastanienbaum, Switzerland
                [3 ]Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern , 3012 Bern, Switzerland
                [4 ]Institute of Evolutionary Biology, University of Edinburgh , Edinburgh EH9 3JY, UK
                [5 ]School of Biological Sciences, University of Auckland , Auckland 1142, New Zealand
                [6 ]Institut des Sciences de l'Evolution UMR 5554, CNRS, IRD, EPHE, Université de Montpellier , 3095 Montpellier cedex 05, France
                Author notes
                Article
                rstb20160455
                10.1098/rstb.2016.0455
                5698618
                29109219
                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                Product
                Funding
                Funded by: Swiss National Science Foundation, http://dx.doi.org/10.13039/501100002848;
                Award ID: 31003A_163446 and 310030E-160812
                Funded by: Royal Society University Research Fellowship;
                Award ID: ISEM 2017-205
                Categories
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                Review Article
                Custom metadata
                December 19, 2017

                Philosophy of science

                genomic architecture, crossing over, meiosis, genetic linkage, evolution, adaptation

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