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A toxin-antidote selfish element increases fitness of its host

Selfish genetic elements can promote their transmission at the expense of individual survival, creating conflict between the element and the rest of the genome. Recently, a large number of toxin-antidote (TA) post-segregation distorters have been identified in non-obligate outcrossing nematodes. The...

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Autores principales: Long, Lijiang, Xu, Wen, Valencia, Francisco, Paaby, Annalise B, McGrath, Patrick T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10629817/
https://www.ncbi.nlm.nih.gov/pubmed/37874324
http://dx.doi.org/10.7554/eLife.81640
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author Long, Lijiang
Xu, Wen
Valencia, Francisco
Paaby, Annalise B
McGrath, Patrick T
author_facet Long, Lijiang
Xu, Wen
Valencia, Francisco
Paaby, Annalise B
McGrath, Patrick T
author_sort Long, Lijiang
collection PubMed
description Selfish genetic elements can promote their transmission at the expense of individual survival, creating conflict between the element and the rest of the genome. Recently, a large number of toxin-antidote (TA) post-segregation distorters have been identified in non-obligate outcrossing nematodes. Their origin and the evolutionary forces that keep them at intermediate population frequencies are poorly understood. Here, we study a TA element in Caenorhabditis elegans called zeel-1;peel-1. Two major haplotypes of this locus, with and without the selfish element, segregate in C. elegans. We evaluate the fitness consequences of the zeel-1;peel-1 element outside of its role in gene drive in non-outcrossing animals and demonstrate that loss of the toxin peel-1 decreased fitness of hermaphrodites and resulted in reductions in fecundity and body size. These findings suggest a biological role for peel-1 beyond toxin lethality. This work demonstrates that a TA element can provide a fitness benefit to its hosts either during their initial evolution or by being co-opted by the animals following their selfish spread. These findings guide our understanding on how TA elements can remain in a population where gene drive is minimized, helping resolve the mystery of prevalent TA elements in selfing animals.
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spelling pubmed-106298172023-11-08 A toxin-antidote selfish element increases fitness of its host Long, Lijiang Xu, Wen Valencia, Francisco Paaby, Annalise B McGrath, Patrick T eLife Evolutionary Biology Selfish genetic elements can promote their transmission at the expense of individual survival, creating conflict between the element and the rest of the genome. Recently, a large number of toxin-antidote (TA) post-segregation distorters have been identified in non-obligate outcrossing nematodes. Their origin and the evolutionary forces that keep them at intermediate population frequencies are poorly understood. Here, we study a TA element in Caenorhabditis elegans called zeel-1;peel-1. Two major haplotypes of this locus, with and without the selfish element, segregate in C. elegans. We evaluate the fitness consequences of the zeel-1;peel-1 element outside of its role in gene drive in non-outcrossing animals and demonstrate that loss of the toxin peel-1 decreased fitness of hermaphrodites and resulted in reductions in fecundity and body size. These findings suggest a biological role for peel-1 beyond toxin lethality. This work demonstrates that a TA element can provide a fitness benefit to its hosts either during their initial evolution or by being co-opted by the animals following their selfish spread. These findings guide our understanding on how TA elements can remain in a population where gene drive is minimized, helping resolve the mystery of prevalent TA elements in selfing animals. eLife Sciences Publications, Ltd 2023-10-24 /pmc/articles/PMC10629817/ /pubmed/37874324 http://dx.doi.org/10.7554/eLife.81640 Text en © 2023, Long et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Long, Lijiang
Xu, Wen
Valencia, Francisco
Paaby, Annalise B
McGrath, Patrick T
A toxin-antidote selfish element increases fitness of its host
title A toxin-antidote selfish element increases fitness of its host
title_full A toxin-antidote selfish element increases fitness of its host
title_fullStr A toxin-antidote selfish element increases fitness of its host
title_full_unstemmed A toxin-antidote selfish element increases fitness of its host
title_short A toxin-antidote selfish element increases fitness of its host
title_sort toxin-antidote selfish element increases fitness of its host
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10629817/
https://www.ncbi.nlm.nih.gov/pubmed/37874324
http://dx.doi.org/10.7554/eLife.81640
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