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Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia

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Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. / Niehuis, Oliver; Gibson, Joshua D.; Rosenberg, Michael S.; Pannebakker, Bart A.; Koevoets, Tosca; Judson, Andrea K.; Desjardins, Christopher A.; Kennedy, Kathleen; Duggan, David; Beukeboom, Leo W.; van de Zande, Louis; Shuker, David Michael; Werren, John H.; Gadau, Juergen.

In: PLoS One, Vol. 5, No. 1, e8597, 19.01.2010.

Research output: Contribution to journalArticle

Harvard

Niehuis, O, Gibson, JD, Rosenberg, MS, Pannebakker, BA, Koevoets, T, Judson, AK, Desjardins, CA, Kennedy, K, Duggan, D, Beukeboom, LW, van de Zande, L, Shuker, DM, Werren, JH & Gadau, J 2010, 'Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia' PLoS One, vol. 5, no. 1, e8597. https://doi.org/10.1371/journal.pone.0008597

APA

Niehuis, O., Gibson, J. D., Rosenberg, M. S., Pannebakker, B. A., Koevoets, T., Judson, A. K., ... Gadau, J. (2010). Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS One, 5(1), [e8597]. https://doi.org/10.1371/journal.pone.0008597

Vancouver

Niehuis O, Gibson JD, Rosenberg MS, Pannebakker BA, Koevoets T, Judson AK et al. Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS One. 2010 Jan 19;5(1). e8597. https://doi.org/10.1371/journal.pone.0008597

Author

Niehuis, Oliver ; Gibson, Joshua D. ; Rosenberg, Michael S. ; Pannebakker, Bart A. ; Koevoets, Tosca ; Judson, Andrea K. ; Desjardins, Christopher A. ; Kennedy, Kathleen ; Duggan, David ; Beukeboom, Leo W. ; van de Zande, Louis ; Shuker, David Michael ; Werren, John H. ; Gadau, Juergen. / Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. In: PLoS One. 2010 ; Vol. 5, No. 1.

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@article{671eef684ad74fd99fc0664894020599,
title = "Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia",
abstract = "Homologous meiotic recombination occurs in most sexually reproducing organisms, yet its evolutionary advantages are elusive. Previous research explored recombination in the honeybee, a eusocial hymenopteran with an exceptionally high genome-wide recombination rate. A comparable study in a non-social member of the Hymenoptera that would disentangle the impact of sociality from Hymenoptera-specific features such as haplodiploidy on the evolution of the high genome-wide recombination rate in social Hymenoptera is missing. Utilizing single-nucleotide polymorphisms (SNPs) between two Nasonia parasitoid wasp genomes, we developed a SNP genotyping microarray to infer a high-density linkage map for Nasonia. The map comprises 1,255 markers with an average distance of 0.3 cM. The mapped markers enabled us to arrange 265 scaffolds of the Nasonia genome assembly 1.0 on the linkage map, representing 63.6{\%} of the assembled N. vitripennis genome. We estimated a genome-wide recombination rate of 1.4-1.5 cM/Mb for Nasonia, which is less than one tenth of the rate reported for the honeybee. The local recombination rate in Nasonia is positively correlated with the distance to the center of the linkage groups, GC content, and the proportion of simple repeats. In contrast to the honeybee genome, gene density in the parasitoid wasp genome is positively associated with the recombination rate; regions of low recombination are characterized by fewer genes with larger introns and by a greater distance between genes. Finally, we found that genes in regions of the genome with a low recombination frequency tend to have a higher ratio of non-synonymous to synonymous substitutions, likely due to the accumulation of slightly deleterious non-synonymous substitutions. These findings are consistent with the hypothesis that recombination reduces interference between linked sites and thereby facilitates adaptive evolution and the purging of deleterious mutations. Our results imply that the genomes of haplodiploid and of diploid higher eukaryotes do not differ systematically in their recombination rates and associated parameters.",
keywords = "Single nucleotide polymorphism, Maximum likelihood models, X-chromosome centromere, Biased gene conversion, Natural selection, Saccharomyces-cerevisiae, Drosophilia melanogaster, Meiotic recombination",
author = "Oliver Niehuis and Gibson, {Joshua D.} and Rosenberg, {Michael S.} and Pannebakker, {Bart A.} and Tosca Koevoets and Judson, {Andrea K.} and Desjardins, {Christopher A.} and Kathleen Kennedy and David Duggan and Beukeboom, {Leo W.} and {van de Zande}, Louis and Shuker, {David Michael} and Werren, {John H.} and Juergen Gadau",
year = "2010",
month = "1",
day = "19",
doi = "10.1371/journal.pone.0008597",
language = "English",
volume = "5",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "1",

}

RIS (suitable for import to EndNote) - Download

TY - JOUR

T1 - Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia

AU - Niehuis, Oliver

AU - Gibson, Joshua D.

AU - Rosenberg, Michael S.

AU - Pannebakker, Bart A.

AU - Koevoets, Tosca

AU - Judson, Andrea K.

AU - Desjardins, Christopher A.

AU - Kennedy, Kathleen

AU - Duggan, David

AU - Beukeboom, Leo W.

AU - van de Zande, Louis

AU - Shuker, David Michael

AU - Werren, John H.

AU - Gadau, Juergen

PY - 2010/1/19

Y1 - 2010/1/19

N2 - Homologous meiotic recombination occurs in most sexually reproducing organisms, yet its evolutionary advantages are elusive. Previous research explored recombination in the honeybee, a eusocial hymenopteran with an exceptionally high genome-wide recombination rate. A comparable study in a non-social member of the Hymenoptera that would disentangle the impact of sociality from Hymenoptera-specific features such as haplodiploidy on the evolution of the high genome-wide recombination rate in social Hymenoptera is missing. Utilizing single-nucleotide polymorphisms (SNPs) between two Nasonia parasitoid wasp genomes, we developed a SNP genotyping microarray to infer a high-density linkage map for Nasonia. The map comprises 1,255 markers with an average distance of 0.3 cM. The mapped markers enabled us to arrange 265 scaffolds of the Nasonia genome assembly 1.0 on the linkage map, representing 63.6% of the assembled N. vitripennis genome. We estimated a genome-wide recombination rate of 1.4-1.5 cM/Mb for Nasonia, which is less than one tenth of the rate reported for the honeybee. The local recombination rate in Nasonia is positively correlated with the distance to the center of the linkage groups, GC content, and the proportion of simple repeats. In contrast to the honeybee genome, gene density in the parasitoid wasp genome is positively associated with the recombination rate; regions of low recombination are characterized by fewer genes with larger introns and by a greater distance between genes. Finally, we found that genes in regions of the genome with a low recombination frequency tend to have a higher ratio of non-synonymous to synonymous substitutions, likely due to the accumulation of slightly deleterious non-synonymous substitutions. These findings are consistent with the hypothesis that recombination reduces interference between linked sites and thereby facilitates adaptive evolution and the purging of deleterious mutations. Our results imply that the genomes of haplodiploid and of diploid higher eukaryotes do not differ systematically in their recombination rates and associated parameters.

AB - Homologous meiotic recombination occurs in most sexually reproducing organisms, yet its evolutionary advantages are elusive. Previous research explored recombination in the honeybee, a eusocial hymenopteran with an exceptionally high genome-wide recombination rate. A comparable study in a non-social member of the Hymenoptera that would disentangle the impact of sociality from Hymenoptera-specific features such as haplodiploidy on the evolution of the high genome-wide recombination rate in social Hymenoptera is missing. Utilizing single-nucleotide polymorphisms (SNPs) between two Nasonia parasitoid wasp genomes, we developed a SNP genotyping microarray to infer a high-density linkage map for Nasonia. The map comprises 1,255 markers with an average distance of 0.3 cM. The mapped markers enabled us to arrange 265 scaffolds of the Nasonia genome assembly 1.0 on the linkage map, representing 63.6% of the assembled N. vitripennis genome. We estimated a genome-wide recombination rate of 1.4-1.5 cM/Mb for Nasonia, which is less than one tenth of the rate reported for the honeybee. The local recombination rate in Nasonia is positively correlated with the distance to the center of the linkage groups, GC content, and the proportion of simple repeats. In contrast to the honeybee genome, gene density in the parasitoid wasp genome is positively associated with the recombination rate; regions of low recombination are characterized by fewer genes with larger introns and by a greater distance between genes. Finally, we found that genes in regions of the genome with a low recombination frequency tend to have a higher ratio of non-synonymous to synonymous substitutions, likely due to the accumulation of slightly deleterious non-synonymous substitutions. These findings are consistent with the hypothesis that recombination reduces interference between linked sites and thereby facilitates adaptive evolution and the purging of deleterious mutations. Our results imply that the genomes of haplodiploid and of diploid higher eukaryotes do not differ systematically in their recombination rates and associated parameters.

KW - Single nucleotide polymorphism

KW - Maximum likelihood models

KW - X-chromosome centromere

KW - Biased gene conversion

KW - Natural selection

KW - Saccharomyces-cerevisiae

KW - Drosophilia melanogaster

KW - Meiotic recombination

UR - http://www.scopus.com/inward/record.url?scp=77649312033&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0008597

DO - 10.1371/journal.pone.0008597

M3 - Article

VL - 5

JO - PLoS One

T2 - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 1

M1 - e8597

ER -

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ID: 2085554