Natural Selection Shapes Variation in Genome-wide Recombination Rate in Drosophila pseudoobscura

AbstractWhile recombination is widely recognized to be a key modulator of numerous evolutionary phenomena, we have a poor understanding of how recombination rate itself varies and evolves within a species. Here, we performed a comprehensive study of recombination rate (rate of meiotic crossing over) in two natural populations of Drosophila pseudoobscura from Utah and Arizona, USA. We used an amplicon sequencing approach to obtain high-quality genotypes in approximately 8000 individual backcrossed offspring (17 mapping populations with roughly 530 individuals each), for which we then quantified crossovers. Interestingly, variation in recombination rate within and between populations largely manifested as differences in genome-wide recombination rate rather than remodeling of the local recombination landscape. Comparing populations, we discovered individuals from the Utah population displayed on average 8% higher crossover rates than the Arizona population, a statistically significant difference. Using a QST-FST analysis, we found that this difference in crossover rate was dramatically higher than expected under neutrality, indicating that this difference may have been driven by natural selection. Finally, using a combination of short and long read whole-genome sequencing, we found no significant association between crossover rate and structural variation at the 200-400kb scale. Our results demonstrate that (1) there is abundant variation in genome-wide crossover rate in natural populations (2) interpopulation differences in recombination rate may be the result of local adaptation, and (3) the observed variation among individuals in recombination rate is primarily driven by global regulators of crossover rate, with little detected variation in recombination rate among strains across specific tracts of individual chromosomes.

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Higher Intercellular Variation in Genome-Wide Recombination Rate in Female Mice

Cytogenetic and Genome Research ◽

10.1159/000516998 ◽

2021 ◽

pp. 1-7

Author(s):

April L. Peterson ◽

Bret A. Payseur

Keyword(s):

Natural Selection ◽

Sex Difference ◽

Meiotic Recombination ◽

Recombination Rate ◽

Inbred Strains ◽

House Mice ◽

Mlh1 Focus ◽

Female Mice ◽

Genome Wide ◽

Recombination Pathway

Meiotic recombination affects fertility, shuffles genomes, and modulates the effectiveness of natural selection. Despite conservation of the recombination pathway, the rate of recombination varies among individuals and along chromosomes. Recombination rate also differs among cells from the same organism, but this form of variation has received less attention. To identify patterns that characterize intercellular variation in the genome-wide recombination rate, we counted foci of the MLH1 recombination-associated protein in oocytes and spermatocytes from a panel of wild-derived inbred strains of house mice. Females show higher intercellular variation in MLH1 focus count than males from the same inbred strains. This pattern is consistent across strains from multiple subspecies, including 2 strains in which the average MLH1 focus count is higher in males. The sex difference in genome-wide recombination rate we report suggests that selection targeting recombination rate will be more efficient in males than in females.

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Faculty Opinions recommendation of Genome-wide inference of natural selection on human transcription factor binding sites.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718018456.793479473 ◽

2013 ◽

Author(s):

Peter Keightley

Keyword(s):

Transcription Factor ◽

Natural Selection ◽

Binding Sites ◽

Transcription Factor Binding Sites ◽

Transcription Factor Binding ◽

Factor Binding ◽

Genome Wide ◽

Human Transcription Factor

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Interactions Between Natural Selection, Recombination and Gene Density in the Genes of Drosophila

Genetics ◽

10.1093/genetics/160.2.595 ◽

2002 ◽

Vol 160 (2) ◽

pp. 595-608 ◽

Cited By ~ 17

Author(s):

Jody Hey ◽

Richard M Kliman

Keyword(s):

Gene Expression ◽

Natural Selection ◽

Recombination Rate ◽

Codon Bias ◽

Gene Density ◽

Drosophila Genome ◽

Functional Variation ◽

Subtle Effect ◽

Efficiency Of Selection ◽

The Impact

AbstractIn Drosophila, as in many organisms, natural selection leads to high levels of codon bias in genes that are highly expressed. Thus codon bias is an indicator of the intensity of one kind of selection that is experienced by genes and can be used to assess the impact of other genomic factors on natural selection. Among 13,000 genes in the Drosophila genome, codon bias has a slight positive, and strongly significant, association with recombination—as expected if recombination allows natural selection to act more efficiently when multiple linked sites segregate functional variation. The same reasoning leads to the expectation that the efficiency of selection, and thus average codon bias, should decline with gene density. However, this prediction is not confirmed. Levels of codon bias and gene expression are highest for those genes in an intermediate range of gene density, a pattern that may be the result of a tradeoff between the advantages for gene expression of close gene spacing and disadvantages arising from regulatory conflicts among tightly packed genes. These factors appear to overlay the more subtle effect of linkage among selected sites that gives rise to the association between recombination rate and codon bias.

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Selfish Genes, Pleiotropy and the Origin of Recombination

Genetics ◽

10.1093/genetics/149.4.2089 ◽

1998 ◽

Vol 149 (4) ◽

pp. 2089-2097 ◽

Cited By ~ 2

Author(s):

Jody Hey

Keyword(s):

Natural Selection ◽

Simple Model ◽

Computer Simulations ◽

Recombination Rate ◽

Evolutionary Origin ◽

Deleterious Mutations ◽

Beneficial Mutations ◽

Selfish Genes ◽

Simple Interaction

Abstract If multiple linked polymorphisms are under natural selection, then conflicts arise and the efficiency of natural selection is hindered relative to the case of no linkage. This simple interaction between linkage and natural selection creates an opportunity for mutations that raise the level of recombination to increase in frequency and have an enhanced chance of fixation. This important finding by S. Otto and N. Barton means that mutations that raise the recombination rate, but are otherwise neutral, will be selectively favored under fairly general circumstances of multilocus selection and linkage. The effect described by Otto and Barton, which was limited to neutral modifiers, can also be extended to include all modifiers of recombination, both beneficial and deleterious. Computer simulations show that beneficial mutations that also increase recombination have an increased chance of fixation. Similarly, deleterious mutations that also decrease recombination have an increased chance of fixation. The results suggest that a simple model of recombination modifiers, including both neutral and pleiotropic modifiers, is a necessary explanation for the evolutionary origin of recombination.

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Role of mutational bias and natural selection on genome-wide nucleotide bias in prokaryotic organisms

Biosystems ◽

10.1016/j.biosystems.2005.01.002 ◽

2005 ◽

Vol 81 (1) ◽

pp. 11-18 ◽

Cited By ~ 18

Author(s):

T. Banerjee ◽

S.K. Gupta ◽

T.C. Ghosh

Keyword(s):

Natural Selection ◽

Mutational Bias ◽

Nucleotide Bias ◽

Genome Wide

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NATURAL SELECTION VS. RANDOM DRIFT: EVIDENCE FROM TEMPORAL VARIATION IN ALLELE FREQUENCIES IN NATURE

Genetics ◽

10.1093/genetics/111.3.517 ◽

1985 ◽

Vol 111 (3) ◽

pp. 517-554

Author(s):

Laurence D Mueller ◽

Lorraine G Barr ◽

Francisco J Ayala

Keyword(s):

Natural Selection ◽

Strong Evidence ◽

Allele Frequencies ◽

Drosophila Pseudoobscura ◽

Frequency Variation ◽

Random Drift ◽

Napa County ◽

Environmental Variations ◽

Monthly Sample ◽

Drosophila Persimilis

ABSTRACT We have obtained monthly samples of two species, Drosophila pseudoobscura and Drosophila persimilis, in a natural population from Napa County, California. In each species, about 300 genes have been assayed by electrophoresis for each of seven enzyme loci in each monthly sample from March 1972 to June 1975. Using statistical methods developed for the purpose, we have examined whether the allele frequencies at different loci vary in a correlated fashion. The methods used do not detect natural selection when it is deterministic (e.g., overdominance or directional selection), but only when alleles at different loci vary simultaneously in response to the same environmental variations. Moreover, only relatively large fitness differences (of the order of 15%) are detectable. We have found strong evidence of correlated allele frequency variation in 13-20% of the cases examined. We interpret this as evidence that natural selection plays a major role in the evolution of protein polymorphisms in nature.

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The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

10.1101/561399 ◽

2019 ◽

Cited By ~ 3

Author(s):

Lewis G. Spurgin ◽

Mirte Bosse ◽

Frank Adriaensen ◽

Tamer Albayrak ◽

Christos Barboutis ◽

...

Keyword(s):

Positive Selection ◽

Recombination Rate ◽

Demographic History ◽

Great Tit ◽

Genomic Variation ◽

Genomic Diversity ◽

Hapmap Project ◽

Widespread Species ◽

Continental Scale ◽

Genome Wide

AbstractA major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear “islands of differentiation” even among populations with very low levels of genome-wide differentiation. Low local recombination rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

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