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Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee

BACKGROUND: Social hymenoptera, the honey bee (Apis mellifera) in particular, have ultra-high crossover rates and a large degree of intra-genomic variation in crossover rates. Aligned with haploid genomics of males, this makes them a potential model for examining the causes and consequences of cross...

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Autores principales: Liu, Haoxuan, Zhang, Xiaohui, Huang, Ju, Chen, Jian-Qun, Tian, Dacheng, Hurst, Laurence D, Yang, Sihai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4305242/
https://www.ncbi.nlm.nih.gov/pubmed/25651211
http://dx.doi.org/10.1186/s13059-014-0566-0
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author Liu, Haoxuan
Zhang, Xiaohui
Huang, Ju
Chen, Jian-Qun
Tian, Dacheng
Hurst, Laurence D
Yang, Sihai
author_facet Liu, Haoxuan
Zhang, Xiaohui
Huang, Ju
Chen, Jian-Qun
Tian, Dacheng
Hurst, Laurence D
Yang, Sihai
author_sort Liu, Haoxuan
collection PubMed
description BACKGROUND: Social hymenoptera, the honey bee (Apis mellifera) in particular, have ultra-high crossover rates and a large degree of intra-genomic variation in crossover rates. Aligned with haploid genomics of males, this makes them a potential model for examining the causes and consequences of crossing over. To address why social insects have such high crossing-over rates and the consequences of this, we constructed a high-resolution recombination atlas by sequencing 55 individuals from three colonies with an average marker density of 314 bp/marker. RESULTS: We find crossing over to be especially high in proximity to genes upregulated in worker brains, but see no evidence for a coupling with immune-related functioning. We detect only a low rate of non-crossover gene conversion, contrary to current evidence. This is in striking contrast to the ultrahigh crossing-over rate, almost double that previously estimated from lower resolution data. We robustly recover the predicted intragenomic correlations between crossing over and both population level diversity and GC content, which could be best explained as indirect and direct consequences of crossing over, respectively. CONCLUSIONS: Our data are consistent with the view that diversification of worker behavior, but not immune function, is a driver of the high crossing-over rate in bees. While we see both high diversity and high GC content associated with high crossing-over rates, our estimate of the low non-crossover rate demonstrates that high non-crossover rates are not a necessary consequence of high recombination rates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-014-0566-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-43052422015-01-25 Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee Liu, Haoxuan Zhang, Xiaohui Huang, Ju Chen, Jian-Qun Tian, Dacheng Hurst, Laurence D Yang, Sihai Genome Biol Research BACKGROUND: Social hymenoptera, the honey bee (Apis mellifera) in particular, have ultra-high crossover rates and a large degree of intra-genomic variation in crossover rates. Aligned with haploid genomics of males, this makes them a potential model for examining the causes and consequences of crossing over. To address why social insects have such high crossing-over rates and the consequences of this, we constructed a high-resolution recombination atlas by sequencing 55 individuals from three colonies with an average marker density of 314 bp/marker. RESULTS: We find crossing over to be especially high in proximity to genes upregulated in worker brains, but see no evidence for a coupling with immune-related functioning. We detect only a low rate of non-crossover gene conversion, contrary to current evidence. This is in striking contrast to the ultrahigh crossing-over rate, almost double that previously estimated from lower resolution data. We robustly recover the predicted intragenomic correlations between crossing over and both population level diversity and GC content, which could be best explained as indirect and direct consequences of crossing over, respectively. CONCLUSIONS: Our data are consistent with the view that diversification of worker behavior, but not immune function, is a driver of the high crossing-over rate in bees. While we see both high diversity and high GC content associated with high crossing-over rates, our estimate of the low non-crossover rate demonstrates that high non-crossover rates are not a necessary consequence of high recombination rates. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-014-0566-0) contains supplementary material, which is available to authorized users. BioMed Central 2015-01-02 2015 /pmc/articles/PMC4305242/ /pubmed/25651211 http://dx.doi.org/10.1186/s13059-014-0566-0 Text en © Liu et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Liu, Haoxuan
Zhang, Xiaohui
Huang, Ju
Chen, Jian-Qun
Tian, Dacheng
Hurst, Laurence D
Yang, Sihai
Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title_full Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title_fullStr Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title_full_unstemmed Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title_short Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
title_sort causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4305242/
https://www.ncbi.nlm.nih.gov/pubmed/25651211
http://dx.doi.org/10.1186/s13059-014-0566-0
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