Genomics of recombination rate variation in temperature-evolved Drosophila melanogaster populations

Abstract Meiotic recombination is a critical process that ensures proper segregation of chromosome homologues through DNA double strand break repair mechanisms. Rates of recombination are highly variable among various taxa, within species, and within genomes with far-reaching evolutionary and genomic consequences. The genetic basis of recombination rate variation is therefore crucial in the study of evolutionary biology but remains poorly understood. In this study we took advantage of a set of experimental temperature-evolved populations of Drosophila melanogaster with heritable differences in recombination rates depending on the temperature regime in which they evolved. We performed whole genome sequencing and identified several chromosomal regions that appear to be divergent depending on temperature regime. In addition, we identify a set of single nucleotide polymorphisms and associated genes with significant differences in allele frequency when the different temperature populations are compared. Further refinement of these gene candidates emphasizing those expressed in the ovary and associated with DNA binding reveals numerous potential candidate genes such as Hr38, EcR, and mamo responsible for observed differences in recombination rates in these experimental evolution lines thus providing insight into the genetic basis of recombination rate variation.

Consequences of Recombination Rate Variation on Quantitative Trait Locus Mapping Studies: Simulations Based on the Drosophila melanogaster Genome

Genetics ◽

10.1093/genetics/159.2.581 ◽

2001 ◽

Vol 159 (2) ◽

pp. 581-588

Author(s):

Mohamed A F Noor ◽

Aimee L Cunningham ◽

John C Larkin

Keyword(s):

Quantitative Trait Locus ◽

Drosophila Melanogaster ◽

Qtl Mapping ◽

Quantitative Trait ◽

Recombination Rate ◽

Genome Project ◽

Gene Density ◽

Rate Variation ◽

Trait Locus ◽

Abstract We examine the effect of variation in gene density per centimorgan on quantitative trait locus (QTL) mapping studies using data from the Drosophila melanogaster genome project and documented regional rates of recombination. There is tremendous variation in gene density per centimorgan across this genome, and we observe that this variation can cause systematic biases in QTL mapping studies. Specifically, in our simulated mapping experiments of 50 equal-effect QTL distributed randomly across the physical genome, very strong QTL are consistently detected near the centromeres of the two major autosomes, and few or no QTL are often detected on the X chromosome. This pattern persisted with varying heritability, marker density, QTL effect sizes, and transgressive segregation. Our results are consistent with empirical data collected from QTL mapping studies of this species and its close relatives, and they explain the “small X-effect” that has been documented in genetic studies of sexual isolation in the D. melanogaster group. Because of the biases resulting from recombination rate variation, results of QTL mapping studies should be taken as hypotheses to be tested by additional genetic methods, particularly in species for which detailed genetic and physical genome maps are not available.

Inferring the Genomic Landscape of Recombination Rate Variation in European Aspen (Populus tremula)

G3 Genes|Genome|Genetics ◽

10.1534/g3.119.400504 ◽

2019 ◽

Vol 10 (1) ◽

pp. 299-309 ◽

Author(s):

Rami-Petteri Apuli ◽

Carolina Bernhardsson ◽

Bastian Schiffthaler ◽

Kathryn M. Robinson ◽

Stefan Jansson ◽

...

Keyword(s):

Linkage Disequilibrium ◽

Linkage Map ◽

Recombination Rate ◽

Gene Density ◽

Populus Tremula ◽

Rate Variation ◽

Recombination Rates ◽

Genomic Features ◽

European Aspen ◽

The rate of meiotic recombination is one of the central factors determining genome-wide levels of linkage disequilibrium which has important consequences for the efficiency of natural selection and for the dissection of quantitative traits. Here we present a new, high-resolution linkage map for Populus tremula that we use to anchor approximately two thirds of the P. tremula draft genome assembly on to the expected 19 chromosomes, providing us with the first chromosome-scale assembly for P. tremula (Table 2). We then use this resource to estimate variation in recombination rates across the P. tremula genome and compare these results to recombination rates based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with a number of genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identifies a number of genomic regions with very high recombination rates that the map-based method fails to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome. Recombination rates are positively correlated with gene density and negatively correlated with repeat density and methylation levels, suggesting that recombination is largely directed toward gene regions in P. tremula.

What drives the evolution of condition-dependent recombination in diploids? Some insights from simulation modelling

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0460 ◽

2017 ◽

Vol 372 (1736) ◽

pp. 20160460 ◽

Cited By ~ 10

Author(s):

Sviatoslav R. Rybnikov ◽

Zeev M. Frenkel ◽

Abraham B. Korol

Keyword(s):

Recombination Rate ◽

External Environment ◽

Theoretical Models ◽

Simulation Modelling ◽

Condition Dependence ◽

Rate Variation ◽

Theoretical Studies ◽

Recombination Rates ◽

Modifier Locus ◽

While the evolutionary advantages of non-zero recombination rates have prompted diverse theoretical explanations, the evolution of essential recombination features remains underexplored. We focused on one such feature, the condition dependence of recombination, viewed as the variation in within-generation sensitivity of recombination to external (environment) and/or internal (genotype) conditions. Limited empirical evidence for its existence comes mainly from diploids, whereas theoretical models show that it only easily evolves in haploids. The evolution of condition-dependent recombination can be explained by its advantage for the selected system (indirect effect), or by benefits to modifier alleles, ensuring this strategy regardless of effects on the selected system (direct effect). We considered infinite panmictic populations of diploids exposed to a cyclical two-state environment. Each organism had three selected loci. Examining allele dynamics at a fourth, selectively neutral recombination modifier locus, we frequently observed that a modifier allele conferring condition-dependent recombination between the selected loci displaced the allele conferring the optimal constant recombination rate. Our simulations also confirm the results of theoretical studies showing that condition-dependent recombination cannot evolve in diploids on the basis of direct fitness-dependent effects alone. Therefore, the evolution of condition-dependent recombination in diploids can be driven by indirect effects alone, i.e. by modifier effects on the selected system. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0455 ◽

2017 ◽

Vol 372 (1736) ◽

pp. 20160455 ◽

Cited By ~ 108

Author(s):

Jessica Stapley ◽

Philine G. D. Feulner ◽

Susan E. Johnston ◽

Anna W. Santure ◽

Carole M. Smadja

Keyword(s):

Recombination Rate ◽

Molecular Mechanisms ◽

Current Knowledge ◽

Essential Feature ◽

Rate Variation ◽

Evolutionary Processes ◽

Recombination Rates ◽

Great Opportunity ◽

Patterns And Processes ◽

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’.

Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee

Molecular Biology and Evolution ◽

10.1093/molbev/msz130 ◽

2019 ◽

Vol 36 (10) ◽

pp. 2277-2291 ◽

Cited By ~ 4

Author(s):

Julia C Jones ◽

Andreas Wallberg ◽

Matthew J Christmas ◽

Karen M Kapheim ◽

Matthew T Webster

Keyword(s):

Recombination Rate ◽

Rate Variation ◽

Sequencing Data ◽

Recombination Rates ◽

Evolution Of Sociality ◽

Leafcutter Bee ◽

Selection For ◽

Worker Caste ◽

Recombination Rate Variation ◽

Genomic Recombination

Abstract Social insect genomes exhibit the highest rates of crossing over observed in plants and animals. The evolutionary causes of these extreme rates are unknown. Insight can be gained by comparing recombination rate variation across the genomes of related social and solitary insects. Here, we compare the genomic recombination landscape of the highly social honey bee, Apis mellifera, with the solitary alfalfa leafcutter bee, Megachile rotundata, by analyzing patterns of linkage disequilibrium in population-scale genome sequencing data. We infer that average recombination rates are extremely elevated in A. mellifera compared with M. rotundata. However, our results indicate that similar factors control the distribution of crossovers in the genomes of both species. Recombination rate is significantly reduced in coding regions in both species, with genes inferred to be germline methylated having particularly low rates. Genes with worker-biased patterns of expression in A. mellifera and their orthologs in M. rotundata have higher than average recombination rates in both species, suggesting that selection for higher diversity in genes involved in worker caste functions in social taxa is not the explanation for these elevated rates. Furthermore, we find no evidence that recombination has modulated the efficacy of selection among genes during bee evolution, which does not support the hypothesis that high recombination rates facilitated positive selection for new functions in social insects. Our results indicate that the evolution of sociality in insects likely entailed selection on modifiers that increased recombination rates genome wide, but that the genomic recombination landscape is determined by the same factors.

Constructing a high-density linkage map to infer the genomic landscape of recombination rate variation in European Aspen (Populus tremula)

10.1101/664037 ◽

2019 ◽

Cited By ~ 1

Author(s):

Rami-Petteri Apuli ◽

Carolina Bernhardsson ◽

Bastian Schiffthaler ◽

Kathryn M. Robinson ◽

Stefan Jansson ◽

...

Keyword(s):

Linkage Disequilibrium ◽

Linkage Map ◽

Recombination Rate ◽

Nucleotide Diversity ◽

Populus Tremula ◽

Rate Variation ◽

Recombination Rates ◽

Genomic Features ◽

European Aspen ◽

AbstractThe rate of meiotic recombination is one of the central factors determining levels of linkage disequilibrium and the efficiency of natural selection, and many organisms show a positive correlation between local rates of recombination and levels of nucleotide diversity indicating that linked selection is an important factor determining genome-wide levels of nucleotide diversity. Several methods for estimating recombination rates from segregating polymorphisms in natural populations have recently been developed. These methods have been extensively used in part because they are relatively simple to implement even in many non-model organisms, but also because they potentially offer higher resolution than traditional map-based methods. However, thorough comparisons of LD and map-based estimates of recombination are not readily available in plants. Here we present a new, high-resolution linkage map for Populus tremula and use this to estimate variation in recombination rates across the P. tremula genome. We compare these results to recombination rates estimated based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identify a number of genomic regions with very high recombination rates that the map-based method fail to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome.

Recombination Rate Variation and Infrequent Sex Influence Genetic Diversity in Chlamydomonas reinhardtii

Genome Biology and Evolution ◽

10.1093/gbe/evaa057 ◽

2020 ◽

Vol 12 (4) ◽

pp. 370-380 ◽

Author(s):

Ahmed R Hasan ◽

Rob W Ness

Keyword(s):

Linkage Disequilibrium ◽

Chlamydomonas Reinhardtii ◽

Recombination Rate ◽

Natural Populations ◽

Effective Rate ◽

Sexual Cycle ◽

Rate Variation ◽

Effective Population ◽

Recombination Rates ◽

Abstract Recombination confers a major evolutionary advantage by breaking up linkage disequilibrium between harmful and beneficial mutations, thereby facilitating selection. However, in species that are only periodically sexual, such as many microbial eukaryotes, the realized rate of recombination is also affected by the frequency of sex, meaning that infrequent sex can increase the effects of selection at linked sites despite high recombination rates. Despite this, the rate of sex of most facultatively sexual species is unknown. Here, we use genomewide patterns of linkage disequilibrium to infer fine-scale recombination rate variation in the genome of the facultatively sexual green alga Chlamydomonas reinhardtii. We observe recombination rate variation of up to two orders of magnitude and find evidence of recombination hotspots across the genome. Recombination rate is highest flanking genes, consistent with trends observed in other nonmammalian organisms, though intergenic recombination rates vary by intergenic tract length. We also find a positive relationship between nucleotide diversity and physical recombination rate, suggesting a widespread influence of selection at linked sites in the genome. Finally, we use estimates of the effective rate of recombination to calculate the rate of sex that occurs in natural populations, estimating a sexual cycle roughly every 840 generations. We argue that the relatively infrequent rate of sex and large effective population size creates a population genetic environment that increases the influence of selection on linked sites across the genome.

Genome-Wide Fine-Scale Recombination Rate Variation in Drosophila melanogaster

PLoS Genetics ◽

10.1371/journal.pgen.1003090 ◽

2012 ◽

Vol 8 (12) ◽

pp. e1003090 ◽

Cited By ~ 146

Author(s):

Andrew H. Chan ◽

Paul A. Jenkins ◽

Yun S. Song

Keyword(s):

Drosophila Melanogaster ◽

Recombination Rate ◽

Rate Variation ◽

Fine Scale ◽

Genome Wide ◽

The Time-Scale of Recombination Rate Evolution in Great Apes

10.1101/013755 ◽

2015 ◽

Author(s):

Laurie S Stevison ◽

August E Woerner ◽

Jeffrey M Kidd ◽

Joanna L Kelley ◽

Krishna R Veeramah ◽

...

Keyword(s):

Recombination Rate ◽

Time Scale ◽

Linear Regression Analysis ◽

Great Apes ◽

Rate Variation ◽

Human Populations ◽

Great Ape ◽

Recombination Rates ◽

Recombination Rate Variation ◽

Broad Scale

We present three linkage-disequilibrium (LD)-based recombination maps generated using whole-genome sequencing data of 10 Nigerian chimpanzees, 13 bonobos, and 15 western gorillas, collected as part of the Great Ape Genome Project (Prado-Martinez et al. 2013). Using species-specific PRDM9 sequences to predict potential binding sites, we identified an important role for PRDM9 in predicting recombination rate variation broadly across great apes. Our results are contrary to previous research that PRDM9 is not associated with recombination in western chimpanzees (Auton et al. 2012). Additionally, we show that fewer hotspots are shared among chimpanzee subspecies than within human populations, further narrowing the time-scale of complete hotspot turnover. We quantified the variation in the biased distribution of recombination rates towards recombination hotspots across great apes. We found that correlations between broad-scale recombination rates decline more rapidly than nucleotide divergence between species. We also compared the skew of recombination rates at centromeres and telomeres between species and show a skew from chromosome means extending as far as 10‐15 Mb from chromosome ends. Further, we examined broad-scale recombination rate changes near a translocation in gorillas and found minimal differences as compared to other great ape species perhaps because the coordinates relative to the chromosome ends were unaffected. Finally, based on multiple linear regression analysis, we found that various correlates of recombination rate persist throughout primates including repeats, diversity, divergence and local effective population size (Ne). Our study is the first to analyze within- and between-species genome-wide recombination rate variation in several close relatives.

DNA motifs are not general predictors of recombination in two Drosophila sister species

10.1101/453639 ◽

2018 ◽

Author(s):

James M. Howie ◽

Rupert Mazzucco ◽

Thomas Taus ◽

Viola Nolte ◽

Christian Schlötterer

Keyword(s):

Recombination Rate ◽

Large Scale ◽

Strong Association ◽

Natural Populations ◽

Sister Species ◽

Rate Variation ◽

Sequence Motifs ◽

Recombination Rates ◽

The Difference ◽

ABSTRACTMeiotic recombination is crucial for chromosomal segregation, and facilitates the spread of beneficial and removal of deleterious mutations. Recombination rates frequently vary along chromosomes and Drosophila melanogaster exhibits a remarkable pattern. Recombination rates gradually decrease towards centromeres and telomeres, with dramatic impact on levels of variation in natural populations. Two close sister species, D. simulans and D. mauritiana do not only have higher recombination rates, but also exhibit a much more homogeneous recombination rate that only drops sharply close to centromeres and telomeres. Because certain sequence motifs are associated with recombination rate variation in D. melanogaster, we tested whether the difference in recombination landscape between D. melanogaster and D. simulans can be explained by the genomic distribution of recombination-rate associated sequence motifs. We constructed the first high resolution recombination map for D. simulans, and searched for motifs linked with high recombination in both sister species. We identified five consensus motifs, present in either species. While the association between motif density and recombination is strong and positive in D. melanogaster, the results are equivocal in D. simulans. Despite the strong association in D. melanogaster, we do not find a decreasing density of these repeat motifs towards centromeres and telomeres. We conclude that the density of recombination-associated repeat motifs cannot explain the large-scale recombination landscape in D. melanogaster, nor the differences to D. simulans. The strong association seen for the sequence motifs in D. melanogaster likely reflects their impact influencing local differences in recombination rates along the genome.