Variation in Recombination Rate Is Shaped by Domestication and Environmental Conditions in Barley

Abstract Meiotic recombination generates genetic diversity upon which selection can act. Recombination rates are highly variable between species, populations, individuals, sexes, chromosomes, and chromosomal regions. The underlying mechanisms are controlled at the genetic and epigenetic level and show plasticity toward the environment. Environmental plasticity may be divided into short- and long-term responses. We estimated recombination rates in natural populations of wild barley and domesticated landraces using a population genetics approach. We analyzed recombination landscapes in wild barley and domesticated landraces at high resolution. In wild barley, high recombination rates are found in more interstitial chromosome regions in contrast to distal chromosome regions in domesticated barley. Among subpopulations of wild barley, natural variation in effective recombination rate is correlated with temperature, isothermality, and solar radiation in a nonlinear manner. A positive linear correlation was found between effective recombination rate and annual precipitation. We discuss our findings with respect to how the environment might shape effective recombination rates in natural populations. Higher recombination rates in wild barley populations subjected to specific environmental conditions could be a means to maintain fitness in a strictly inbreeding species.

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Restriction Fragment Length Polymorphism and Divergence in the Genomic Regions of High and Low Recombination in Self-Fertilizing and Cross-Fertilizing Aegilops Species

Genetics ◽

10.1093/genetics/148.1.423 ◽

1998 ◽

Vol 148 (1) ◽

pp. 423-434

Author(s):

Jan Dvorřák ◽

Ming-Cheng Luo ◽

Zu-Li Yang

Keyword(s):

Related Species ◽

Gene Diversity ◽

Single Copy ◽

Species Variation ◽

Recombination Rates ◽

Distal Chromosome ◽

Phylogenetic Status ◽

Average Gene ◽

Genomic Regions ◽

Chromosome Regions

Abstract RFLP was investigated at 52 single-copy gene loci among six species of Aegilops, including both cross-fertilizing and self-fertilizing species. Average gene diversity (H) was found to correlate with the level of outcrossing. No relationship was found between H and the phylogenetic status of a species. In all six species, the level of RFLP at a locus was a function of the position of the locus on the chromosome and the recombination rate in the neighborhood of the locus. Loci in the proximal chromosome regions, which show greatly reduced recombination rates relative to the distal regions, were significantly less variable than loci in the distal chromosome regions in all six species. Variation in recombination rates was also reflected in the haplotype divergence between closely related species; loci in the chromosome regions with low recombination rates were found to be diverged less than those in the chromosome regions with high recombination rates. This relationship was not found among the more distantly related species.

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Gene buddies: Linked balanced polymorphisms reinforce each other even in the absence of epistasis

10.1101/220897 ◽

2017 ◽

Author(s):

Jacob A Tennessen

Keyword(s):

Recombination Rate ◽

Evolutionary Dynamics ◽

Balancing Selection ◽

Natural Populations ◽

Adaptive Variation ◽

Recombination Rates ◽

Future Studies ◽

Close Physical Proximity ◽

Selection For ◽

Independent Effects

The fates of genetic polymorphisms maintained by balancing selection depend on evolutionary dynamics at linked sites. While coevolution across linked, epigenetically-interacting loci has been extensively explored, such supergenes may be relatively rare. However, genes harboring adaptive variation can occur in close physical proximity while generating independent effects on fitness. Here, I present a model in which two linked loci without epistasis are both under balancing selection for unrelated reasons. Using forward-time simulations, I show that recombination rate strongly influences the retention of adaptive polymorphism, especially for intermediate selection coefficients. A locus is more likely to retain adaptive variation if it is closely linked to another locus under balancing selection, even if the two loci have no interaction. Thus, two linked polymorphisms can both be retained indefinitely even when they would both be lost to drift if unlinked. Such clusters of mutually reinforcing genes may underlie phenotypic variation in natural populations. Future studies that measure selection coefficients and recombination rates among closely linked genes will be fruitful for characterizing the extent of this phenomenon.

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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 ◽

Cited By ~ 2

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 ◽

Recombination Rate Variation

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.

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Selective Sweeps in the Presence of Interference Among Partially Linked Loci

Genetics ◽

10.1093/genetics/164.1.389 ◽

2003 ◽

Vol 164 (1) ◽

pp. 389-398 ◽

Cited By ~ 1

Author(s):

Yuseob Kim ◽

Wolfgang Stephan

Keyword(s):

Genetic Variation ◽

Recombination Rate ◽

Substantial Reduction ◽

Natural Populations ◽

High Rate ◽

Selective Sweeps ◽

Recombination Rates ◽

Analytical Approximations ◽

Fixation Probabilities ◽

Beneficial Allele

Abstract Recurrent directional selection on a partially recombining chromosome may cause a substantial reduction of standing genetic variation in natural populations. Previous studies of this effect, commonly called selective sweeps, assumed that at most one beneficial allele is on the way to fixation at a given time. However, for a high rate of selected substitutions and a low recombination rate, this assumption can easily be violated. We investigated this problem using full-forward simulations and analytical approximations. We found that interference between linked beneficial alleles causes a reduction of their fixation probabilities. The hitchhiking effect on linked neutral variation for a given substitution also slightly decreases due to interference. As a result, the strength of recurrent selective sweeps is weakened. However, this effect is significant only in chromosomal regions of relatively low recombination rates where the level of variation is greatly reduced. Therefore, previous results on recurrent selective sweeps although derived for a restricted parameter range are still valid. Analytical approximations are obtained for the case of complete linkage for which interference between competing beneficial alleles is maximal.

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Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution

Science Advances ◽

10.1126/sciadv.abg5285 ◽

2021 ◽

Vol 7 (25) ◽

pp. eabg5285

Author(s):

Garrett A. Roberts Kingman ◽

Deven N. Vyas ◽

Felicity C. Jones ◽

Shannon D. Brady ◽

Heidi I. Chen ◽

...

Keyword(s):

Natural Populations ◽

Composite Model ◽

Large Set ◽

Recombination Rates ◽

Genomic Features ◽

Freshwater Habitats ◽

Repeated Evolution ◽

Frequency Changes ◽

Underlying Mechanisms ◽

Genomic Basis

Similar forms often evolve repeatedly in nature, raising long-standing questions about the underlying mechanisms. Here, we use repeated evolution in stickleback to identify a large set of genomic loci that change recurrently during colonization of freshwater habitats by marine fish. The same loci used repeatedly in extant populations also show rapid allele frequency changes when new freshwater populations are experimentally established from marine ancestors. Marked genotypic and phenotypic changes arise within 5 years, facilitated by standing genetic variation and linkage between adaptive regions. Both the speed and location of changes can be predicted using empirical observations of recurrence in natural populations or fundamental genomic features like allelic age, recombination rates, density of divergent loci, and overlap with mapped traits. A composite model trained on these stickleback features can also predict the location of key evolutionary loci in Darwin’s finches, suggesting that similar features are important for evolution across diverse taxa.

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Gene flow biases population genetic inference of recombination rate

10.1101/2021.09.26.461846 ◽

2021 ◽

Author(s):

Kieran Samuk ◽

Mohamed A.F. Noor

Keyword(s):

Gene Flow ◽

Recombination Rate ◽

Population Genetic ◽

Natural Populations ◽

Recombination Rates ◽

False Negatives ◽

Isolation With Migration ◽

Simplifying Assumptions ◽

Population Genetic Inference ◽

Genetic Inference

Accurate estimates of the rate of recombination are key to understanding a host of evolutionary processes as well as the evolution of recombination rate itself. Model-based population genetic methods that infer recombination rates from patterns of linkage disequilibrium (LD) in the genome have become a popular method to estimate rates of recombination. However, these LD-based methods make a variety of simplifying assumptions about the populations of interest that are often not met in natural populations. One such assumption is the absence of gene flow from other populations. Here, we use forward-time population genetic simulations of isolation-with-migration scenarios to explore how gene flow affects the accuracy of LD-based estimators of recombination rate. We find that moderate levels of gene flow can result in either the overestimation or underestimation of recombination rates by up to 20-50% depending on the timing of divergence. We also find that these biases can affect the detection of interpopulation differences in recombination rate, causing both false positive and false negatives depending on the scenario. We discuss future possibilities for mitigating these biases and recommend that investigators exercise caution and confirm that their study populations meet assumptions before deploying these methods.

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Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution

10.1101/2020.11.13.382424 ◽

2020 ◽

Author(s):

Garrett A Roberts Kingman ◽

Deven N Vyas ◽

Felicity C Jones ◽

Shannon D Brady ◽

Heidi I Chen ◽

...

Keyword(s):

Natural Populations ◽

Composite Model ◽

Large Set ◽

Recombination Rates ◽

Genomic Features ◽

Freshwater Habitats ◽

Repeated Evolution ◽

Frequency Changes ◽

Underlying Mechanisms ◽

Genomic Basis

AbstractSimilar forms often evolve repeatedly in nature, raising longstanding questions about the underlying mechanisms. Here we use repeated evolution in sticklebacks to identify a large set of genomic loci that change recurrently during colonization of new freshwater habitats by marine fish. The same loci used repeatedly in extant populations also show rapid allele frequency changes when new freshwater populations are experimentally established from marine ancestors. Dramatic genotypic and phenotypic changes arise within 5-7 years, facilitated by standing genetic variation and linkage between adaptive regions. Both the speed and location of changes can be predicted using empirical observations of recurrence in natural populations or fundamental genomic features like allelic age, recombination rates, density of divergent loci, and overlap with mapped traits. A composite model trained on these stickleback features can also predict the location of key evolutionary loci in Darwin’s finches, suggesting similar features are important for evolution across diverse taxa.

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

10.1101/453639 ◽

2018 ◽

Cited By ~ 2

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 ◽

Recombination Rate Variation

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.

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Microsatellite Variation and Recombination Rate in the Human Genome

Genetics ◽

10.1093/genetics/156.3.1285 ◽

2000 ◽

Vol 156 (3) ◽

pp. 1285-1298 ◽

Cited By ~ 3

Author(s):

Bret A Payseur ◽

Michael W Nachman

Keyword(s):

Recombination Rate ◽

Microsatellite Polymorphism ◽

Published Data ◽

Strong Positive Correlation ◽

Background Selection ◽

Recombination Rates ◽

Microsatellite Variation ◽

Positive Correlation ◽

Genome Recombination ◽

Neutral Mutations

Abstract Background (purifying) selection on deleterious mutations is expected to remove linked neutral mutations from a population, resulting in a positive correlation between recombination rate and levels of neutral genetic variation, even for markers with high mutation rates. We tested this prediction of the background selection model by comparing recombination rate and levels of microsatellite polymorphism in humans. Published data for 28 unrelated Europeans were used to estimate microsatellite polymorphism (number of alleles, heterozygosity, and variance in allele size) for loci throughout the genome. Recombination rates were estimated from comparisons of genetic and physical maps. First, we analyzed 61 loci from chromosome 22, using the complete sequence of this chromosome to provide exact physical locations. These 61 microsatellites showed no correlation between levels of variation and recombination rate. We then used radiation-hybrid and cytogenetic maps to calculate recombination rates throughout the genome. Recombination rates varied by more than one order of magnitude, and most chromosomes showed significant suppression of recombination near the centromere. Genome-wide analyses provided no evidence for a strong positive correlation between recombination rate and polymorphism, although analyses of loci with at least 20 repeats suggested a weak positive correlation. Comparisons of microsatellites in lowest-recombination and highest-recombination regions also revealed no difference in levels of polymorphism. Together, these results indicate that background selection is not a major determinant of microsatellite variation in humans.

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Patterns of DNA Variability at X-Linked Loci in Mus domesticus

Genetics ◽

10.1093/genetics/147.3.1303 ◽

1997 ◽

Vol 147 (3) ◽

pp. 1303-1316

Author(s):

Michael W Nachman

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

House Mouse ◽

Recombination Rate ◽

Nucleotide Diversity ◽

Mus Domesticus ◽

Substantial Variation ◽

Intraspecific Polymorphism ◽

Recombination Rates ◽

Interspecific Divergence

Introns of four X-linked genes (Hprt, Plp, Glra2, and Amg) were sequenced to provide an estimate of nucleotide diversity at nuclear genes within the house mouse and to test the neutral prediction that the ratio of intraspecific polymorphism to interspecific divergence is the same for different loci. Hprt and Plp lie in a region of the X chromosome that experiences relatively low recombination rates, while Glra2 and Amg lie near the telomere of the X chromosome, a region that experiences higher recombination rates. A total of 6022 bases were sequenced in each of 10 Mus domesticus and one M. caroli. Average nucleotide diversity (π) for introns within M. domesticus was quite low (π = 0.078%). However, there was substantial variation in the level of heterozygosity among loci. The two telomeric loci, Glra2 and Amg, had higher ratios of polymorphism to divergence than the two loci experiencing lower recombination rates. These results are consistent with the hypothesis that heterozygosity is reduced in regions with lower rates of recombination, although sampling of additional genes is needed to establish whether there is a general correlation between heterozygosity and recombination rate as in Drosophila melanogaster.

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