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Conservation of the genome-wide recombination rate in white-footed mice.

ABSTRACT: Despite being linked to the fundamental processes of chromosome segregation and offspring diversification, meiotic recombination rates vary within and between species. Recent years have seen progress in quantifying recombination rate evolution across multiple temporal and genomic scales. Nevertheless, the level of variation in recombination rate within wild populations-a key determinant of evolution in this trait-remains poorly documented on the genomic scale. To address this notable gap, we used immunofluorescent cytology to quantify genome-wide recombination rates in males from a wild population of the white-footed mouse, Peromyscus leucopus. For comparison, we measured recombination rates in a second population of male P. leucopus raised in the laboratory and in male deer mice from the subspecies Peromyscus maniculatus bairdii. Although we found differences between individuals in the genome-wide recombination rate, levels of variation were low-within populations, between populations, and between species. Quantification of synaptonemal complex length and crossover positions along chromosome 1 using a novel automated approach also revealed conservation in broad-scale crossover patterning, including strong crossover interference. We propose stabilizing selection targeting recombination or correlated processes as the explanation for these patterns.

SUBMITTER: Peterson AL

PROVIDER: S-EPMC6781155 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Conservation of the genome-wide recombination rate in white-footed mice.

Peterson April L AL Miller Nathan D ND Payseur Bret A BA

Heredity 20190731 4

Despite being linked to the fundamental processes of chromosome segregation and offspring diversification, meiotic recombination rates vary within and between species. Recent years have seen progress in quantifying recombination rate evolution across multiple temporal and genomic scales. Nevertheless, the level of variation in recombination rate within wild populations-a key determinant of evolution in this trait-remains poorly documented on the genomic scale. To address this notable gap, we use ...[more]

PMID: 31366913

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Project description:Meiotic recombination is a fundamental evolutionary process. It not only generates diversity, but influences the efficacy of natural selection and genome evolution. There can be significant heterogeneity in recombination rates within and between species, however this variation is not well understood outside of a few model taxa, particularly in forest trees. Eucalypts are forest trees of global economic importance, and dominate many Australian ecosystems. We studied recombination rate in Eucalyptus globulus using genetic linkage maps constructed in 10 unrelated individuals, and markers anchored to the Eucalyptus reference genome. This experimental design provided the replication to study whether recombination rate varied between individuals and chromosomes, and allowed us to study the genomic attributes and population genetic parameters correlated with this variation.Recombination rate varied significantly between individuals (range?=?2.71 to 3.51 centimorgans/megabase [cM/Mb]), but was not significantly influenced by sex or cross type (F1 vs. F2). Significant differences in recombination rate between chromosomes were also evident (range?=?1.98 to 3.81 cM/Mb), beyond those which were due to variation in chromosome size. Variation in chromosomal recombination rate was significantly correlated with gene density (r?=?0.94), GC content (r?=?0.90), and the number of tandem duplicated genes (r?=?-0.72) per chromosome. Notably, chromosome level recombination rate was also negatively correlated with the average genetic diversity across six species from an independent set of samples (r?=?-0.75).The correlations with genomic attributes are consistent with findings in other taxa, however, the direction of the correlation between diversity and recombination rate is opposite to that commonly observed. We argue this is likely to reflect the interaction of selection and specific genome architecture of Eucalyptus. Interestingly, the differences amongst chromosomes in recombination rates appear stable across Eucalyptus species. Together with the strong correlations between recombination rate and features of the Eucalyptus reference genome, we maintain these findings provide further evidence for a broad conservation of genome architecture across the globally significant lineages of Eucalyptus.

Project description:Estimating fine-scale recombination maps of Drosophila from population genomic data is a challenging problem, in particular because of the high background recombination rate. In this paper, a new computational method is developed to address this challenge. Through an extensive simulation study, it is demonstrated that the method allows more accurate inference, and exhibits greater robustness to the effects of natural selection and noise, compared to a well-used previous method developed for studying fine-scale recombination rate variation in the human genome. As an application, a genome-wide analysis of genetic variation data is performed for two Drosophila melanogaster populations, one from North America (Raleigh, USA) and the other from Africa (Gikongoro, Rwanda). It is shown that fine-scale recombination rate variation is widespread throughout the D. melanogaster genome, across all chromosomes and in both populations. At the fine-scale, a conservative, systematic search for evidence of recombination hotspots suggests the existence of a handful of putative hotspots each with at least a tenfold increase in intensity over the background rate. A wavelet analysis is carried out to compare the estimated recombination maps in the two populations and to quantify the extent to which recombination rates are conserved. In general, similarity is observed at very broad scales, but substantial differences are seen at fine scales. The average recombination rate of the X chromosome appears to be higher than that of the autosomes in both populations, and this pattern is much more pronounced in the African population than the North American population. The correlation between various genomic features-including recombination rates, diversity, divergence, GC content, gene content, and sequence quality-is examined using the wavelet analysis, and it is shown that the most notable difference between D. melanogaster and humans is in the correlation between recombination and diversity.

Dataset Information

Conservation of the genome-wide recombination rate in white-footed mice.

Publications

Conservation of the genome-wide recombination rate in white-footed mice.

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