Selfing is the safest sex for Caenorhabditis tropicalis

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the le...

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Main Authors: Luke M Noble, John Yuen, Lewis Stevens, Nicolas Moya, Riaad Persaud, Marc Moscatelli, Jacqueline L Jackson, Gaotian Zhang, Rojin Chitrakar, L Ryan Baugh, Christian Braendle, Erik C Andersen, Hannah S Seidel, Matthew V Rockman
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/62587
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author Luke M Noble
John Yuen
Lewis Stevens
Nicolas Moya
Riaad Persaud
Marc Moscatelli
Jacqueline L Jackson
Gaotian Zhang
Rojin Chitrakar
L Ryan Baugh
Christian Braendle
Erik C Andersen
Hannah S Seidel
Matthew V Rockman
author_facet Luke M Noble
John Yuen
Lewis Stevens
Nicolas Moya
Riaad Persaud
Marc Moscatelli
Jacqueline L Jackson
Gaotian Zhang
Rojin Chitrakar
L Ryan Baugh
Christian Braendle
Erik C Andersen
Hannah S Seidel
Matthew V Rockman
author_sort Luke M Noble
collection DOAJ
description Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.
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spelling doaj.art-509875295c34445da55a4dc6ea6c29d52022-12-22T03:24:43ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.62587Selfing is the safest sex for Caenorhabditis tropicalisLuke M Noble0https://orcid.org/0000-0002-5161-4059John Yuen1https://orcid.org/0000-0002-1569-3298Lewis Stevens2https://orcid.org/0000-0002-6075-8273Nicolas Moya3https://orcid.org/0000-0002-6817-1784Riaad Persaud4Marc Moscatelli5Jacqueline L Jackson6https://orcid.org/0000-0001-5376-0968Gaotian Zhang7Rojin Chitrakar8L Ryan Baugh9https://orcid.org/0000-0003-2148-5492Christian Braendle10Erik C Andersen11https://orcid.org/0000-0003-0229-9651Hannah S Seidel12Matthew V Rockman13https://orcid.org/0000-0001-6492-8906Department of Biology and Center for Genomics & Systems Biology, New York University, New York, United States; Institute de Biologie, École Normale Supérieure, CNRS, Inserm, Paris, FranceDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Biology, Duke University, Durham, United StatesDepartment of Biology, Duke University, Durham, United StatesInstitut de Biologie Valrose, Université Côte d’Azur, CNRS, Inserm, Nice, FranceDepartment of Molecular Biosciences, Northwestern University, Evanston, United StatesDepartment of Biology, Eastern Michigan University, Ypsilanti, United StatesDepartment of Biology and Center for Genomics & Systems Biology, New York University, New York, United StatesMating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.https://elifesciences.org/articles/62587caenorhabditis tropicalisselfingmating systemsbalancing selectiongene drivepopulation genetics
spellingShingle Luke M Noble
John Yuen
Lewis Stevens
Nicolas Moya
Riaad Persaud
Marc Moscatelli
Jacqueline L Jackson
Gaotian Zhang
Rojin Chitrakar
L Ryan Baugh
Christian Braendle
Erik C Andersen
Hannah S Seidel
Matthew V Rockman
Selfing is the safest sex for Caenorhabditis tropicalis
eLife
caenorhabditis tropicalis
selfing
mating systems
balancing selection
gene drive
population genetics
title Selfing is the safest sex for Caenorhabditis tropicalis
title_full Selfing is the safest sex for Caenorhabditis tropicalis
title_fullStr Selfing is the safest sex for Caenorhabditis tropicalis
title_full_unstemmed Selfing is the safest sex for Caenorhabditis tropicalis
title_short Selfing is the safest sex for Caenorhabditis tropicalis
title_sort selfing is the safest sex for caenorhabditis tropicalis
topic caenorhabditis tropicalis
selfing
mating systems
balancing selection
gene drive
population genetics
url https://elifesciences.org/articles/62587
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