Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.

The neotropical Drosophila paulistorum superspecies, consisting of at least six geographically overlapping but reproductively isolated semispecies, has been the object of extensive research since at least 1955, when it was initially trapped mid-evolution in flagrant statu nascendi. In this classic s...

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Autores principales: Wolfgang J Miller, Lee Ehrman, Daniela Schneider
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Publicado: Public Library of Science (PLoS) 2010
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spelling oai:doaj.org-article:7f32153cbece4387bbc943177575e8ff2021-11-18T06:03:46ZInfectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.1553-73661553-737410.1371/journal.ppat.1001214https://doaj.org/article/7f32153cbece4387bbc943177575e8ff2010-12-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21151959/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The neotropical Drosophila paulistorum superspecies, consisting of at least six geographically overlapping but reproductively isolated semispecies, has been the object of extensive research since at least 1955, when it was initially trapped mid-evolution in flagrant statu nascendi. In this classic system females express strong premating isolation patterns against mates belonging to any other semispecies, and yet uncharacterized microbial reproductive tract symbionts were described triggering hybrid inviability and male sterility. Based on theoretical models and limited experimental data, prime candidates fostering symbiont-driven speciation in arthropods are intracellular bacteria belonging to the genus Wolbachia. They are maternally inherited symbionts of many arthropods capable of manipulating host reproductive biology for their own benefits. However, it is an ongoing debate as to whether or not reproductive symbionts are capable of driving host speciation in nature and if so, to what extent. Here we have reevaluated this classic case of infectious speciation by means of present day molecular approaches and artificial symbiont depletion experiments. We have isolated the α-proteobacteria Wolbachia as the maternally transmitted core endosymbionts of all D. paulistorum semispecies that have coevolved towards obligate mutualism with their respective native hosts. In hybrids, however, these mutualists transform into pathogens by overreplication causing embryonic inviability and male sterility. We show that experimental reduction in native Wolbachia titer causes alterations in sex ratio, fecundity, and mate discrimination. Our results indicate that formerly designated Mycoplasma-like organisms are most likely Wolbachia that have evolved by becoming essential mutualistic symbionts in their respective natural hosts; they have the potential to trigger pre- and postmating isolation. Furthermore, in light of our new findings, we revisit the concept of infectious speciation and discuss potential mechanisms that can restrict or promote symbiont-induced speciation at post- and prezygotic levels in nature and under artificial laboratory conditions.Wolfgang J MillerLee EhrmanDaniela SchneiderPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 6, Iss 12, p e1001214 (2010)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Wolfgang J Miller
Lee Ehrman
Daniela Schneider
Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
description The neotropical Drosophila paulistorum superspecies, consisting of at least six geographically overlapping but reproductively isolated semispecies, has been the object of extensive research since at least 1955, when it was initially trapped mid-evolution in flagrant statu nascendi. In this classic system females express strong premating isolation patterns against mates belonging to any other semispecies, and yet uncharacterized microbial reproductive tract symbionts were described triggering hybrid inviability and male sterility. Based on theoretical models and limited experimental data, prime candidates fostering symbiont-driven speciation in arthropods are intracellular bacteria belonging to the genus Wolbachia. They are maternally inherited symbionts of many arthropods capable of manipulating host reproductive biology for their own benefits. However, it is an ongoing debate as to whether or not reproductive symbionts are capable of driving host speciation in nature and if so, to what extent. Here we have reevaluated this classic case of infectious speciation by means of present day molecular approaches and artificial symbiont depletion experiments. We have isolated the α-proteobacteria Wolbachia as the maternally transmitted core endosymbionts of all D. paulistorum semispecies that have coevolved towards obligate mutualism with their respective native hosts. In hybrids, however, these mutualists transform into pathogens by overreplication causing embryonic inviability and male sterility. We show that experimental reduction in native Wolbachia titer causes alterations in sex ratio, fecundity, and mate discrimination. Our results indicate that formerly designated Mycoplasma-like organisms are most likely Wolbachia that have evolved by becoming essential mutualistic symbionts in their respective natural hosts; they have the potential to trigger pre- and postmating isolation. Furthermore, in light of our new findings, we revisit the concept of infectious speciation and discuss potential mechanisms that can restrict or promote symbiont-induced speciation at post- and prezygotic levels in nature and under artificial laboratory conditions.
format article
author Wolfgang J Miller
Lee Ehrman
Daniela Schneider
author_facet Wolfgang J Miller
Lee Ehrman
Daniela Schneider
author_sort Wolfgang J Miller
title Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
title_short Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
title_full Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
title_fullStr Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
title_full_unstemmed Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum.
title_sort infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of drosophila paulistorum.
publisher Public Library of Science (PLoS)
publishDate 2010
url https://doaj.org/article/7f32153cbece4387bbc943177575e8ff
work_keys_str_mv AT wolfgangjmiller infectiousspeciationrevisitedimpactofsymbiontdepletiononfemalefitnessandmatingbehaviorofdrosophilapaulistorum
AT leeehrman infectiousspeciationrevisitedimpactofsymbiontdepletiononfemalefitnessandmatingbehaviorofdrosophilapaulistorum
AT danielaschneider infectiousspeciationrevisitedimpactofsymbiontdepletiononfemalefitnessandmatingbehaviorofdrosophilapaulistorum
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