Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>

ABSTRACT Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (C...

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Autores principales:	Emily M. Layton, Jungmin On, Jessamyn I. Perlmutter, Seth R. Bordenstein, J. Dylan Shropshire
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Wolbachia Drosophila melanogaster cytoplasmic incompatibility maternal transmission Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/87cd3693f61f458a9478c8656c090b4a
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spelling	oai:doaj.org-article:87cd3693f61f458a9478c8656c090b4a2021-11-15T15:54:46ZPaternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>10.1128/mBio.01879-192150-7511https://doaj.org/article/87cd3693f61f458a9478c8656c090b4a2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01879-19https://doaj.org/toc/2150-7511ABSTRACT Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the “paternal grandmother age effect” (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model. IMPORTANCE Unidirectional cytoplasmic incompatibility (CI) results in a postfertilization incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.Emily M. LaytonJungmin OnJessamyn I. PerlmutterSeth R. BordensteinJ. Dylan ShropshireAmerican Society for MicrobiologyarticleWolbachiaDrosophila melanogastercytoplasmic incompatibilitymaternal transmissionMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Wolbachia Drosophila melanogaster cytoplasmic incompatibility maternal transmission Microbiology QR1-502
spellingShingle	Wolbachia Drosophila melanogaster cytoplasmic incompatibility maternal transmission Microbiology QR1-502 Emily M. Layton Jungmin On Jessamyn I. Perlmutter Seth R. Bordenstein J. Dylan Shropshire Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
description	ABSTRACT Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including cytoplasmic incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the “paternal grandmother age effect” (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model. IMPORTANCE Unidirectional cytoplasmic incompatibility (CI) results in a postfertilization incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.
format	article
author	Emily M. Layton Jungmin On Jessamyn I. Perlmutter Seth R. Bordenstein J. Dylan Shropshire
author_facet	Emily M. Layton Jungmin On Jessamyn I. Perlmutter Seth R. Bordenstein J. Dylan Shropshire
author_sort	Emily M. Layton
title	Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_short	Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full	Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_fullStr	Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_full_unstemmed	Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>
title_sort	paternal grandmother age affects the strength of <italic toggle="yes">wolbachia</italic>-induced cytoplasmic incompatibility in <named-content content-type="genus-species">drosophila melanogaster</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/87cd3693f61f458a9478c8656c090b4a
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Paternal Grandmother Age Affects the Strength of <italic toggle="yes">Wolbachia</italic>-Induced Cytoplasmic Incompatibility in <named-content content-type="genus-species">Drosophila melanogaster</named-content>

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