Recombination Suppression is Unlikely to Contribute to Speciation in Sympatric Heliconius Butterflies

AbstractMechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of co-adapted gene combinations. The sympatric butterfly species H. melpomene and H. cydno are separated by many strong barriers, but the species still hybridise infrequently in the wild, with around 40% of the genome influenced by introgression. We tested the hypothesis that genetic barriers between the species are reinforced by inversions or other mechanisms to reduce between-species recombination rate. We constructed fine-scale recombination maps for Panamanian populations of both species and hybrids to directly measure recombination rate between these species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.Author SummaryIt is now possible to study the process of species formation by sequencing the genomes of multiple closely related species. Heliconius melpomene and Heliconius cydno are two butterfly species that have diverged over the past 2 million years and have different colour patterns, mate preferences and host plants. However, they still hybridise infrequently in the wild and exchange large parts of their genomes. Typically, when genomes are exchanged, chromosomes are recombined and gene combinations are broken up, preventing species from forming. Theory predicts that gene variants that define species might be linked together because of structural differences in their genomes, such as inverted pieces of chromosomes that will not be broken up when the species hybridise. However, in this paper, we use deep sequencing of large crosses of butterflies to show that there are no long chromosome regions that are not broken up during hybridisation, and no long chromosome inversions anywhere between the two genomes. This suggests that hybridisation is rare enough and mate preference is strong enough that inversions are not necessary to maintain the species barrier.

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Negative heterosis for meiotic recombination rate in spermatocytes of the domestic chicken Gallus gallus

Vavilov Journal of Genetics and Breeding ◽

10.18699/vj21.075 ◽

2021 ◽

Vol 25 (6) ◽

pp. 661-668

Author(s):

L. P. Malinovskaya ◽

K. V. Tishakova ◽

T. I. Bikchurina ◽

A. Yu. Slobodchikova ◽

N. Yu. Torgunakov ◽

...

Keyword(s):

Dna Sequences ◽

Meiotic Recombination ◽

Recombination Rate ◽

F1 Hybrids ◽

Dna Breaks ◽

Recombination Rates ◽

Recombination Nodules ◽

Double Strand Dna Breaks ◽

Repair Protein ◽

Benefits And Costs

Benefits and costs of meiotic recombination are a matter of discussion. Because recombination breaks allele combinations already tested by natural selection and generates new ones of unpredictable fitness, a high recombination rate is generally beneficial for the populations living in a fluctuating or a rapidly changing environment and costly in a stable environment. Besides genetic benefits and costs, there are cytological effects of recombination, both positive and negative. Recombination is necessary for chromosome synapsis and segregation. However, it involves a massive generation of double-strand DNA breaks, erroneous repair of which may lead to germ cell death or various mutations and chromosome rearrangements. Thus, the benefits of recombination (generation of new allele combinations) would prevail over its costs (occurrence of deleterious mutations) as long as the population remains sufficiently heterogeneous. Using immunolocalization of MLH1, a mismatch repair protein, at the synaptonemal complexes, we examined the number and distribution of recombination nodules in spermatocytes of two chicken breeds with high (Pervomai) and low (Russian Crested) recombination rates and their F1 hybrids and backcrosses. We detected negative heterosis for recombination rate in the F1 hybrids. Backcrosses to the Pervomai breed were rather homogenous and showed an intermediate recombination rate. The differences in overall recombination rate between the breeds, hybrids and backcrosses were mainly determined by the differences in the crossing over number in the seven largest macrochromosomes. The decrease in recombination rate in F1 is probably determined by difficulties in homology matching between the DNA sequences of genetically divergent breeds. The suppression of recombination in the hybrids may impede gene flow between parapatric populations and therefore accelerate their genetic divergence.

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Effects of Mutations of RAD50, RAD51, RAD52, and Related Genes on Illegitimate Recombination in Saccharomyces cerevisiae

Genetics ◽

10.1093/genetics/142.2.383 ◽

1996 ◽

Vol 142 (2) ◽

pp. 383-391 ◽

Cited By ~ 2

Author(s):

Yasumasa Tsukamoto ◽

Jun-ichi Kato ◽

Hideo Ikeda

Keyword(s):

Saccharomyces Cerevisiae ◽

Quantitative Analysis ◽

Structural Analysis ◽

Recombination Rate ◽

Type Strain ◽

Negative Selection ◽

Wild Type Strain ◽

Illegitimate Recombination ◽

Wild Type ◽

In The Wild

Abstract To examine the mechanism of illegitimate recombination in Saccharomyces cerevisiae, we have developed a plasmid system for quantitative analysis of deletion formation. A can1 cyh2 cell carrying two negative selection markers, the CAN1 and CYH2 genes, on a YCp plasmid is sensitive to canavanine and cycloheximide, but the cell becomes resistant to both drugs when the plasmid has a deletion over the CAN1 and CYH2 genes. Structural analysis of the recombinant plasmids obtained from the resistant cells showed that the plasmids had deletions at various sites of the CAN1-CYH2 region and there were only short regions of homology (1-5 bp) at the recombination junctions. The results indicated that the deletion detected in this system were formed by illegitimate recombination. Study on the effect of several rad mutations showed that the recombination rate was reduced by 30-, 10-, 10-, and 10-fold in the rad52, rad50, mre11, and xrs2 mutants, respectively, while in the rud51, 54, 55, and 57 mutants, the rate was comparable to that in the wild-type strain. The rad52 mutation did not affect length of homology at junction sites of illegitimate recombination.

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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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Modeling Linkage Disequilibrium and Identifying Recombination Hotspots Using Single-Nucleotide Polymorphism Data

Genetics ◽

10.1093/genetics/165.4.2213 ◽

2003 ◽

Vol 165 (4) ◽

pp. 2213-2233 ◽

Cited By ~ 41

Author(s):

Na Li ◽

Matthew Stephens

Keyword(s):

Linkage Disequilibrium ◽

Recombination Rate ◽

Population Sample ◽

Simulated Data ◽

Region Of Interest ◽

Population Data ◽

Recombination Rates ◽

Single Nucleotide ◽

Recombination Hotspots ◽

Genomic Regions

AbstractWe introduce a new statistical model for patterns of linkage disequilibrium (LD) among multiple SNPs in a population sample. The model overcomes limitations of existing approaches to understanding, summarizing, and interpreting LD by (i) relating patterns of LD directly to the underlying recombination process; (ii) considering all loci simultaneously, rather than pairwise; (iii) avoiding the assumption that LD necessarily has a “block-like” structure; and (iv) being computationally tractable for huge genomic regions (up to complete chromosomes). We examine in detail one natural application of the model: estimation of underlying recombination rates from population data. Using simulation, we show that in the case where recombination is assumed constant across the region of interest, recombination rate estimates based on our model are competitive with the very best of current available methods. More importantly, we demonstrate, on real and simulated data, the potential of the model to help identify and quantify fine-scale variation in recombination rate from population data. We also outline how the model could be useful in other contexts, such as in the development of more efficient haplotype-based methods for LD mapping.

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Mutation rate analysis via parent–progeny sequencing of the perennial peach. II. No evidence for recombination-associated mutation

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.1785 ◽

2016 ◽

Vol 283 (1841) ◽

pp. 20161785 ◽

Cited By ~ 4

Author(s):

Long Wang ◽

Yanchun Zhang ◽

Chao Qin ◽

Dacheng Tian ◽

Sihai Yang ◽

...

Keyword(s):

Mutation Rate ◽

Recombination Rate ◽

Mutation Rates ◽

Recombination Rates ◽

Rate Analysis ◽

A Genome ◽

Break Points ◽

New Mutations

Mutation rates and recombination rates vary between species and between regions within a genome. What are the determinants of these forms of variation? Prior evidence has suggested that the recombination might be mutagenic with an excess of new mutations in the vicinity of recombination break points. As it is conjectured that domesticated taxa have higher recombination rates than wild ones, we expect domesticated taxa to have raised mutation rates. Here, we use parent–offspring sequencing in domesticated and wild peach to ask (i) whether recombination is mutagenic, and (ii) whether domesticated peach has a higher recombination rate than wild peach. We find no evidence that domesticated peach has an increased recombination rate, nor an increased mutation rate near recombination events. If recombination is mutagenic in this taxa, the effect is too weak to be detected by our analysis. While an absence of recombination-associated mutation might explain an absence of a recombination–heterozygozity correlation in peach, we caution against such an interpretation.

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The Theory and Applications of Measuring Broad-Range and Chromosome-Wide Recombination Rate from Allele Frequency Decay around a Selected Locus

Molecular Biology and Evolution ◽

10.1093/molbev/msaa171 ◽

2020 ◽

Vol 37 (12) ◽

pp. 3654-3671

Author(s):

Kevin H -C Wei ◽

Aditya Mantha ◽

Doris Bachtrog

Keyword(s):

Genetic Distance ◽

Allele Frequency ◽

Recombination Rate ◽

High Throughput Sequencing ◽

Genetic Material ◽

Cost Effective ◽

Genetic Distances ◽

Recombination Rates ◽

Marker Selection ◽

Cost Effective Approach

Abstract Recombination is the exchange of genetic material between homologous chromosomes via physical crossovers. High-throughput sequencing approaches detect crossovers genome wide to produce recombination rate maps but are difficult to scale as they require large numbers of recombinants individually sequenced. We present a simple and scalable pooled-sequencing approach to experimentally infer near chromosome-wide recombination rates by taking advantage of non-Mendelian allele frequency generated from a fitness differential at a locus under selection. As more crossovers decouple the selected locus from distal loci, the distorted allele frequency attenuates distally toward Mendelian and can be used to estimate the genetic distance. Here, we use marker selection to generate distorted allele frequency and theoretically derive the mathematical relationships between allele frequency attenuation, genetic distance, and recombination rate in marker-selected pools. We implemented nonlinear curve-fitting methods that robustly estimate the allele frequency decay from batch sequencing of pooled individuals and derive chromosome-wide genetic distance and recombination rates. Empirically, we show that marker-selected pools closely recapitulate genetic distances inferred from scoring recombinants. Using this method, we generated novel recombination rate maps of three wild-derived strains of Drosophila melanogaster, which strongly correlate with previous measurements. Moreover, we show that this approach can be extended to estimate chromosome-wide crossover interference with reciprocal marker selection and discuss how it can be applied in the absence of visible markers. Altogether, we find that our method is a simple and cost-effective approach to generate chromosome-wide recombination rate maps requiring only one or two libraries.

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

Molecular Biology and Evolution ◽

10.1093/molbev/msz141 ◽

2019 ◽

Vol 36 (9) ◽

pp. 2029-2039 ◽

Cited By ~ 4

Author(s):

Steven Dreissig ◽

Martin Mascher ◽

Stefan Heckmann

Keyword(s):

Environmental Conditions ◽

Recombination Rate ◽

Wild Barley ◽

Natural Populations ◽

Recombination Rates ◽

Distal Chromosome ◽

Positive Linear Correlation ◽

Short And Long Term ◽

Underlying Mechanisms ◽

Chromosome Regions

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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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 ◽

Cited By ~ 2

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 ◽

Recombination Rate Variation

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.

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Risk of social colours in an agamid lizard: implications for the evolution of dynamic signals

Biology Letters ◽

10.1098/rsbl.2019.0207 ◽

2019 ◽

Vol 15 (5) ◽

pp. 20190207 ◽

Cited By ~ 2

Author(s):

Madhura S. Amdekar ◽

Maria Thaker

Keyword(s):

Natural Selection ◽

Social Interactions ◽

Predation Risk ◽

Colour Pattern ◽

Male Aggression ◽

Visual Systems ◽

In The Wild ◽

Predation Costs ◽

Colour Patterns ◽

Ecological Cost

The forces of sexual and natural selection are typically invoked to explain variation in colour patterns of animals. Although the benefits of conspicuous colours for social signalling are well documented, evidence for their ecological cost, especially for dynamic colours, remains limited. We examined the riskiness of colour patterns of Psammophilus dorsalis , a species in which males express distinct colour combinations during social interactions. We first measured the conspicuousness of these colour patterns on different substrates based on the visual systems of conspecifics and predators (bird, snake, canid) and then quantified actual predation risk on these patterns using wax/polymer lizard models in the wild. The black and red male state exhibited during courtship was the most conspicuous to all visual systems, while the yellow and orange male aggression state and the brown female colour were least conspicuous. Models bearing the courtship colour pattern experienced the highest predator attacks, irrespective of the substrate they were placed on. Thus, social colours of males are not only conspicuous but also risky. Using physiological colours to shift in and out of conspicuous states may be an effective evolutionary solution to balance social signalling benefits with predation costs.

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