Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica

Abstract The maintenance of sex is paradoxical as sexual species pay the “twofold cost of males” and should thus quickly be replaced by asexual mutants reproducing clonally. However, asexuals may not be strictly clonal and engage in “cryptic sex,” challenging this simple scenario. We study the crypt...

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Main Authors: Loreleï Boyer, Roula Jabbour‐Zahab, Marta Mosna, Christoph R. Haag, Thomas Lenormand
Format: Article
Language:English
Published: Oxford University Press 2021-04-01
Series:Evolution Letters
Subjects:
Online Access:https://doi.org/10.1002/evl3.216
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author Loreleï Boyer
Roula Jabbour‐Zahab
Marta Mosna
Christoph R. Haag
Thomas Lenormand
author_facet Loreleï Boyer
Roula Jabbour‐Zahab
Marta Mosna
Christoph R. Haag
Thomas Lenormand
author_sort Loreleï Boyer
collection DOAJ
description Abstract The maintenance of sex is paradoxical as sexual species pay the “twofold cost of males” and should thus quickly be replaced by asexual mutants reproducing clonally. However, asexuals may not be strictly clonal and engage in “cryptic sex,” challenging this simple scenario. We study the cryptic sex life of the brine shrimp Artemia parthenogenetica, which has once been termed an “ancient asexual” and where no genetic differences have ever been observed between parents and offspring. This asexual species rarely produces males, which can hybridize with sexual females of closely related species and transmit asexuality to their offspring. Using such hybrids, we show that recombination occurs in asexual lineages, causing loss‐of‐heterozygosity and parent‐offspring differences. These differences cannot generally be observed in field‐sampled asexuals because once heterozygosity is lost, subsequent recombination leaves no footprint. Furthermore, using extensive paternity tests, we show that hybrid females can reproduce both sexually and asexually, and transmit asexuality to both sexually and asexually produced offspring in a dominant fashion. Finally, we show that, contrary to previous reports, field‐sampled asexual females also rarely reproduce sexually (rate ∼2‰). Overall, most previously known facts about Artemia asexuality turned out to be erroneous. More generally, our findings suggest that the evidence for strictly clonal reproduction of asexual species needs to be reconsidered, and that rare sex and consequences of nonclonal asexuality, such as gene flow within asexuals, need to be more widely taken into account in more realistic models for the maintenance of sex and the persistence of asexual lineages.
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spelling doaj.art-1f4a817c9d4c4aae83fc29076e7ed37f2023-09-02T10:57:00ZengOxford University PressEvolution Letters2056-37442021-04-015216417410.1002/evl3.216Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogeneticaLoreleï Boyer0Roula Jabbour‐Zahab1Marta Mosna2Christoph R. Haag3Thomas Lenormand4CEFE Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD Montpellier FranceCEFE Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD Montpellier FranceCEFE Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD Montpellier FranceCEFE Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD Montpellier FranceCEFE Univ Montpellier, CNRS, Univ Paul Valéry Montpellier 3, EPHE, IRD Montpellier FranceAbstract The maintenance of sex is paradoxical as sexual species pay the “twofold cost of males” and should thus quickly be replaced by asexual mutants reproducing clonally. However, asexuals may not be strictly clonal and engage in “cryptic sex,” challenging this simple scenario. We study the cryptic sex life of the brine shrimp Artemia parthenogenetica, which has once been termed an “ancient asexual” and where no genetic differences have ever been observed between parents and offspring. This asexual species rarely produces males, which can hybridize with sexual females of closely related species and transmit asexuality to their offspring. Using such hybrids, we show that recombination occurs in asexual lineages, causing loss‐of‐heterozygosity and parent‐offspring differences. These differences cannot generally be observed in field‐sampled asexuals because once heterozygosity is lost, subsequent recombination leaves no footprint. Furthermore, using extensive paternity tests, we show that hybrid females can reproduce both sexually and asexually, and transmit asexuality to both sexually and asexually produced offspring in a dominant fashion. Finally, we show that, contrary to previous reports, field‐sampled asexual females also rarely reproduce sexually (rate ∼2‰). Overall, most previously known facts about Artemia asexuality turned out to be erroneous. More generally, our findings suggest that the evidence for strictly clonal reproduction of asexual species needs to be reconsidered, and that rare sex and consequences of nonclonal asexuality, such as gene flow within asexuals, need to be more widely taken into account in more realistic models for the maintenance of sex and the persistence of asexual lineages.https://doi.org/10.1002/evl3.216Artemiaasexualsautomixiscontagious asexualityrare sexrecombination
spellingShingle Loreleï Boyer
Roula Jabbour‐Zahab
Marta Mosna
Christoph R. Haag
Thomas Lenormand
Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
Evolution Letters
Artemia
asexuals
automixis
contagious asexuality
rare sex
recombination
title Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
title_full Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
title_fullStr Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
title_full_unstemmed Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
title_short Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica
title_sort not so clonal asexuals unraveling the secret sex life of artemia parthenogenetica
topic Artemia
asexuals
automixis
contagious asexuality
rare sex
recombination
url https://doi.org/10.1002/evl3.216
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