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Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?

Reproductive isolation in response to divergent selection is often mediated via third‐party interactions. Under these conditions, speciation is inextricably linked to ecological context. We present a novel framework for understanding arthropod speciation as mediated by Wolbachia, a microbial endosym...

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Autores principales: Darwell, Clive T., Souto‐Vilarós, Daniel, Michalek, Jan, Boutsi, Sotiria, Isua, Brus, Sisol, Mentap, Kuyaiva, Thomas, Weiblen, George, Křivan, Vlastimil, Novotny, Vojtech, Segar, Simon T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006231/
https://www.ncbi.nlm.nih.gov/pubmed/35432921
http://dx.doi.org/10.1002/ece3.8826
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author Darwell, Clive T.
Souto‐Vilarós, Daniel
Michalek, Jan
Boutsi, Sotiria
Isua, Brus
Sisol, Mentap
Kuyaiva, Thomas
Weiblen, George
Křivan, Vlastimil
Novotny, Vojtech
Segar, Simon T.
author_facet Darwell, Clive T.
Souto‐Vilarós, Daniel
Michalek, Jan
Boutsi, Sotiria
Isua, Brus
Sisol, Mentap
Kuyaiva, Thomas
Weiblen, George
Křivan, Vlastimil
Novotny, Vojtech
Segar, Simon T.
author_sort Darwell, Clive T.
collection PubMed
description Reproductive isolation in response to divergent selection is often mediated via third‐party interactions. Under these conditions, speciation is inextricably linked to ecological context. We present a novel framework for understanding arthropod speciation as mediated by Wolbachia, a microbial endosymbiont capable of causing host cytoplasmic incompatibility (CI). We predict that sympatric host sister‐species harbor paraphyletic Wolbachia strains that provide CI, while well‐defined congeners in ecological contact and recently diverged noninteracting congeners are uninfected due to Wolbachia redundancy. We argue that Wolbachia provides an adaptive advantage when coupled with reduced hybrid fitness, facilitating assortative mating between co‐occurring divergent phenotypes—the contact contingency hypothesis. To test this, we applied a predictive algorithm to empirical pollinating fig wasp data, achieving up to 91.60% accuracy. We further postulate that observed temporal decay of Wolbachia incidence results from adaptive host purging—adaptive decay hypothesis—but implementation failed to predict systematic patterns. We then account for post‐zygotic offspring mortality during CI mating, modeling fitness clines across developmental resources—the fecundity trade‐off hypothesis. This model regularly favored CI despite fecundity losses. We demonstrate that a rules‐based algorithm accurately predicts Wolbachia infection status. This has implications among other systems where closely related sympatric species encounter adaptive disadvantage through hybridization.
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spelling pubmed-90062312022-04-15 Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom? Darwell, Clive T. Souto‐Vilarós, Daniel Michalek, Jan Boutsi, Sotiria Isua, Brus Sisol, Mentap Kuyaiva, Thomas Weiblen, George Křivan, Vlastimil Novotny, Vojtech Segar, Simon T. Ecol Evol Research Articles Reproductive isolation in response to divergent selection is often mediated via third‐party interactions. Under these conditions, speciation is inextricably linked to ecological context. We present a novel framework for understanding arthropod speciation as mediated by Wolbachia, a microbial endosymbiont capable of causing host cytoplasmic incompatibility (CI). We predict that sympatric host sister‐species harbor paraphyletic Wolbachia strains that provide CI, while well‐defined congeners in ecological contact and recently diverged noninteracting congeners are uninfected due to Wolbachia redundancy. We argue that Wolbachia provides an adaptive advantage when coupled with reduced hybrid fitness, facilitating assortative mating between co‐occurring divergent phenotypes—the contact contingency hypothesis. To test this, we applied a predictive algorithm to empirical pollinating fig wasp data, achieving up to 91.60% accuracy. We further postulate that observed temporal decay of Wolbachia incidence results from adaptive host purging—adaptive decay hypothesis—but implementation failed to predict systematic patterns. We then account for post‐zygotic offspring mortality during CI mating, modeling fitness clines across developmental resources—the fecundity trade‐off hypothesis. This model regularly favored CI despite fecundity losses. We demonstrate that a rules‐based algorithm accurately predicts Wolbachia infection status. This has implications among other systems where closely related sympatric species encounter adaptive disadvantage through hybridization. John Wiley and Sons Inc. 2022-04-13 /pmc/articles/PMC9006231/ /pubmed/35432921 http://dx.doi.org/10.1002/ece3.8826 Text en © 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Darwell, Clive T.
Souto‐Vilarós, Daniel
Michalek, Jan
Boutsi, Sotiria
Isua, Brus
Sisol, Mentap
Kuyaiva, Thomas
Weiblen, George
Křivan, Vlastimil
Novotny, Vojtech
Segar, Simon T.
Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title_full Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title_fullStr Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title_full_unstemmed Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title_short Predicting distributions of Wolbachia strains through host ecological contact—Who's manipulating whom?
title_sort predicting distributions of wolbachia strains through host ecological contact—who's manipulating whom?
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006231/
https://www.ncbi.nlm.nih.gov/pubmed/35432921
http://dx.doi.org/10.1002/ece3.8826
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