Cargando…

A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review

Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independentl...

Descripción completa

Detalles Bibliográficos
Autores principales: Russell, Jacob A., Funaro, Colin F., Giraldo, Ysabel M., Goldman-Huertas, Benjamin, Suh, David, Kronauer, Daniel J. C., Moreau, Corrie S., Pierce, Naomi E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3527441/
https://www.ncbi.nlm.nih.gov/pubmed/23284655
http://dx.doi.org/10.1371/journal.pone.0051027
_version_ 1782253723613921280
author Russell, Jacob A.
Funaro, Colin F.
Giraldo, Ysabel M.
Goldman-Huertas, Benjamin
Suh, David
Kronauer, Daniel J. C.
Moreau, Corrie S.
Pierce, Naomi E.
author_facet Russell, Jacob A.
Funaro, Colin F.
Giraldo, Ysabel M.
Goldman-Huertas, Benjamin
Suh, David
Kronauer, Daniel J. C.
Moreau, Corrie S.
Pierce, Naomi E.
author_sort Russell, Jacob A.
collection PubMed
description Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independently evolved a heritable lifestyle, less is known about their host ranges. Moreover, most groups of insects have not had their heritable microflora systematically surveyed across a broad range of their taxonomic diversity. To help remedy these shortcomings we used diagnostic PCR to screen for five groups of heritable symbionts—Arsenophonus spp., Cardinium hertigii, Hamiltonella defensa, Spiroplasma spp., and Wolbachia spp.—across the ants and lepidopterans (focusing, in the latter case, on two butterfly families—the Lycaenidae and Nymphalidae). We did not detect Cardinium or Hamiltonella in any host. Wolbachia were the most widespread, while Spiroplasma (ants and lepidopterans) and Arsenophonus (ants only) were present at low levels. Co-infections with different Wolbachia strains appeared especially common in ants and less so in lepidopterans. While no additional facultative heritable symbionts were found among ants using universal bacterial primers, microbes related to heritable enteric bacteria were detected in several hosts. In summary, our findings show that Wolbachia are the dominant heritable symbionts of ants and at least some lepidopterans. However, a systematic review of symbiont frequencies across host taxa revealed that this is not always the case across other arthropods. Furthermore, comparisons of symbiont frequencies revealed that the prevalence of Wolbachia and other heritable symbionts varies substantially across lower-level arthropod taxa. We discuss the correlates, potential causes, and implications of these patterns, providing hypotheses on host attributes that may shape the distributions of these influential bacteria.
format Online
Article
Text
id pubmed-3527441
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-35274412013-01-02 A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review Russell, Jacob A. Funaro, Colin F. Giraldo, Ysabel M. Goldman-Huertas, Benjamin Suh, David Kronauer, Daniel J. C. Moreau, Corrie S. Pierce, Naomi E. PLoS One Research Article Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independently evolved a heritable lifestyle, less is known about their host ranges. Moreover, most groups of insects have not had their heritable microflora systematically surveyed across a broad range of their taxonomic diversity. To help remedy these shortcomings we used diagnostic PCR to screen for five groups of heritable symbionts—Arsenophonus spp., Cardinium hertigii, Hamiltonella defensa, Spiroplasma spp., and Wolbachia spp.—across the ants and lepidopterans (focusing, in the latter case, on two butterfly families—the Lycaenidae and Nymphalidae). We did not detect Cardinium or Hamiltonella in any host. Wolbachia were the most widespread, while Spiroplasma (ants and lepidopterans) and Arsenophonus (ants only) were present at low levels. Co-infections with different Wolbachia strains appeared especially common in ants and less so in lepidopterans. While no additional facultative heritable symbionts were found among ants using universal bacterial primers, microbes related to heritable enteric bacteria were detected in several hosts. In summary, our findings show that Wolbachia are the dominant heritable symbionts of ants and at least some lepidopterans. However, a systematic review of symbiont frequencies across host taxa revealed that this is not always the case across other arthropods. Furthermore, comparisons of symbiont frequencies revealed that the prevalence of Wolbachia and other heritable symbionts varies substantially across lower-level arthropod taxa. We discuss the correlates, potential causes, and implications of these patterns, providing hypotheses on host attributes that may shape the distributions of these influential bacteria. Public Library of Science 2012-12-20 /pmc/articles/PMC3527441/ /pubmed/23284655 http://dx.doi.org/10.1371/journal.pone.0051027 Text en © 2012 Russell et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Russell, Jacob A.
Funaro, Colin F.
Giraldo, Ysabel M.
Goldman-Huertas, Benjamin
Suh, David
Kronauer, Daniel J. C.
Moreau, Corrie S.
Pierce, Naomi E.
A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title_full A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title_fullStr A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title_full_unstemmed A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title_short A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
title_sort veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3527441/
https://www.ncbi.nlm.nih.gov/pubmed/23284655
http://dx.doi.org/10.1371/journal.pone.0051027
work_keys_str_mv AT russelljacoba averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT funarocolinf averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT giraldoysabelm averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT goldmanhuertasbenjamin averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT suhdavid averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT kronauerdanieljc averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT moreaucorries averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT piercenaomie averitablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT russelljacoba veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT funarocolinf veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT giraldoysabelm veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT goldmanhuertasbenjamin veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT suhdavid veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT kronauerdanieljc veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT moreaucorries veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview
AT piercenaomie veritablemenagerieofheritablebacteriafromantsbutterfliesandbeyondbroadmolecularsurveysandasystematicreview