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Balancing selection maintains hyper-divergent haplotypes in C. elegans

Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times. The transition from outcrossing to selfing significantly decreases the effective population size, effective recombination rate, and heterozygosity within a species. These changes lead to a re...

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Autores principales: Lee, Daehan, Zdraljevic, Stefan, Stevens, Lewis, Wang, Ye, Tanny, Robyn E., Crombie, Timothy A., Cook, Daniel E., Webster, Amy K., Chirakar, Rojin, Baugh, L. Ryan, Sterken, Mark G., Braendle, Christian, Félix, Marie-Anne, Rockman, Matthew V., Andersen, Erik C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8202730/
https://www.ncbi.nlm.nih.gov/pubmed/33820969
http://dx.doi.org/10.1038/s41559-021-01435-x
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author Lee, Daehan
Zdraljevic, Stefan
Stevens, Lewis
Wang, Ye
Tanny, Robyn E.
Crombie, Timothy A.
Cook, Daniel E.
Webster, Amy K.
Chirakar, Rojin
Baugh, L. Ryan
Sterken, Mark G.
Braendle, Christian
Félix, Marie-Anne
Rockman, Matthew V.
Andersen, Erik C.
author_facet Lee, Daehan
Zdraljevic, Stefan
Stevens, Lewis
Wang, Ye
Tanny, Robyn E.
Crombie, Timothy A.
Cook, Daniel E.
Webster, Amy K.
Chirakar, Rojin
Baugh, L. Ryan
Sterken, Mark G.
Braendle, Christian
Félix, Marie-Anne
Rockman, Matthew V.
Andersen, Erik C.
author_sort Lee, Daehan
collection PubMed
description Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times. The transition from outcrossing to selfing significantly decreases the effective population size, effective recombination rate, and heterozygosity within a species. These changes lead to a reduction in genetic diversity, and therefore adaptive potential, by intensifying the effects of random genetic drift and linked selection. Within the nematode genus Caenorhabditis, selfing has evolved at least three times and all three species, including in the model organism Caenorhabditis elegans, show substantially reduced genetic diversity relative to outcrossing species. Selfing and outcrossing Caenorhabditis species are often found in the same niches, but we still do not know how selfing species with limited genetic diversity can adapt to these environments. Here, we examine the whole-genome sequences from 609 wild C. elegans strains isolated worldwide and show that genetic variation is concentrated in punctuated hyper-divergent regions that cover 20% of the C. elegans reference genome. These regions are enriched in environmental response genes that mediate sensory perception, pathogen response, and xenobiotic stress response. Population genomic evidence suggests that genetic diversity in these regions has been maintained by long-term balancing selection. Using long- read genome assemblies for 15 wild strains, we show that hyper-divergent haplotypes contain unique sets of genes and show levels of divergence comparable to levels found between Caenorhabditis species that diverged millions of years ago. These results provide an example for how species can avoid the evolutionary “dead end” associated with selfing.
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spelling pubmed-82027302021-10-05 Balancing selection maintains hyper-divergent haplotypes in C. elegans Lee, Daehan Zdraljevic, Stefan Stevens, Lewis Wang, Ye Tanny, Robyn E. Crombie, Timothy A. Cook, Daniel E. Webster, Amy K. Chirakar, Rojin Baugh, L. Ryan Sterken, Mark G. Braendle, Christian Félix, Marie-Anne Rockman, Matthew V. Andersen, Erik C. Nat Ecol Evol Article Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times. The transition from outcrossing to selfing significantly decreases the effective population size, effective recombination rate, and heterozygosity within a species. These changes lead to a reduction in genetic diversity, and therefore adaptive potential, by intensifying the effects of random genetic drift and linked selection. Within the nematode genus Caenorhabditis, selfing has evolved at least three times and all three species, including in the model organism Caenorhabditis elegans, show substantially reduced genetic diversity relative to outcrossing species. Selfing and outcrossing Caenorhabditis species are often found in the same niches, but we still do not know how selfing species with limited genetic diversity can adapt to these environments. Here, we examine the whole-genome sequences from 609 wild C. elegans strains isolated worldwide and show that genetic variation is concentrated in punctuated hyper-divergent regions that cover 20% of the C. elegans reference genome. These regions are enriched in environmental response genes that mediate sensory perception, pathogen response, and xenobiotic stress response. Population genomic evidence suggests that genetic diversity in these regions has been maintained by long-term balancing selection. Using long- read genome assemblies for 15 wild strains, we show that hyper-divergent haplotypes contain unique sets of genes and show levels of divergence comparable to levels found between Caenorhabditis species that diverged millions of years ago. These results provide an example for how species can avoid the evolutionary “dead end” associated with selfing. 2021-04-05 2021-06 /pmc/articles/PMC8202730/ /pubmed/33820969 http://dx.doi.org/10.1038/s41559-021-01435-x Text en http://www.nature.com/authors/editorial_policies/license.html#termsUsers may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Lee, Daehan
Zdraljevic, Stefan
Stevens, Lewis
Wang, Ye
Tanny, Robyn E.
Crombie, Timothy A.
Cook, Daniel E.
Webster, Amy K.
Chirakar, Rojin
Baugh, L. Ryan
Sterken, Mark G.
Braendle, Christian
Félix, Marie-Anne
Rockman, Matthew V.
Andersen, Erik C.
Balancing selection maintains hyper-divergent haplotypes in C. elegans
title Balancing selection maintains hyper-divergent haplotypes in C. elegans
title_full Balancing selection maintains hyper-divergent haplotypes in C. elegans
title_fullStr Balancing selection maintains hyper-divergent haplotypes in C. elegans
title_full_unstemmed Balancing selection maintains hyper-divergent haplotypes in C. elegans
title_short Balancing selection maintains hyper-divergent haplotypes in C. elegans
title_sort balancing selection maintains hyper-divergent haplotypes in c. elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8202730/
https://www.ncbi.nlm.nih.gov/pubmed/33820969
http://dx.doi.org/10.1038/s41559-021-01435-x
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