Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.

Wolbachia are maternally inherited symbiotic bacteria, commonly found in arthropods, which are able to manipulate the reproduction of their host in order to maximise their transmission. The evolutionary history of endosymbionts like Wolbachia can be revealed by integrating information on infection s...

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Main Authors: Mark F Richardson, Lucy A Weinert, John J Welch, Raquel S Linheiro, Michael M Magwire, Francis M Jiggins, Casey M Bergman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003129&type=printable
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author Mark F Richardson
Lucy A Weinert
John J Welch
Raquel S Linheiro
Michael M Magwire
Francis M Jiggins
Casey M Bergman
author_facet Mark F Richardson
Lucy A Weinert
John J Welch
Raquel S Linheiro
Michael M Magwire
Francis M Jiggins
Casey M Bergman
author_sort Mark F Richardson
collection DOAJ
description Wolbachia are maternally inherited symbiotic bacteria, commonly found in arthropods, which are able to manipulate the reproduction of their host in order to maximise their transmission. The evolutionary history of endosymbionts like Wolbachia can be revealed by integrating information on infection status in natural populations with patterns of sequence variation in Wolbachia and host mitochondrial genomes. Here we use whole-genome resequencing data from 290 lines of Drosophila melanogaster from North America, Europe, and Africa to predict Wolbachia infection status, estimate relative cytoplasmic genome copy number, and reconstruct Wolbachia and mitochondrial genome sequences. Overall, 63% of Drosophila strains were predicted to be infected with Wolbachia by our in silico analysis pipeline, which shows 99% concordance with infection status determined by diagnostic PCR. Complete Wolbachia and mitochondrial genomes show congruent phylogenies, consistent with strict vertical transmission through the maternal cytoplasm and imperfect transmission of Wolbachia. Bayesian phylogenetic analysis reveals that the most recent common ancestor of all Wolbachia and mitochondrial genomes in D. melanogaster dates to around 8,000 years ago. We find evidence for a recent global replacement of ancestral Wolbachia and mtDNA lineages, but our data suggest that the derived wMel lineage arose several thousand years ago, not in the 20th century as previously proposed. Our data also provide evidence that this global replacement event is incomplete and is likely to be one of several similar incomplete replacement events that have occurred since the out-of-Africa migration that allowed D. melanogaster to colonize worldwide habitats. This study provides a complete genomic analysis of the evolutionary mode and temporal dynamics of the D. melanogaster-Wolbachia symbiosis, as well as important resources for further analyses of the impact of Wolbachia on host biology.
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spelling doaj-art-bd8fdebdf71744f9913c9fb7442289d32025-08-20T03:01:15ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-01812e100312910.1371/journal.pgen.1003129Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.Mark F RichardsonLucy A WeinertJohn J WelchRaquel S LinheiroMichael M MagwireFrancis M JigginsCasey M BergmanWolbachia are maternally inherited symbiotic bacteria, commonly found in arthropods, which are able to manipulate the reproduction of their host in order to maximise their transmission. The evolutionary history of endosymbionts like Wolbachia can be revealed by integrating information on infection status in natural populations with patterns of sequence variation in Wolbachia and host mitochondrial genomes. Here we use whole-genome resequencing data from 290 lines of Drosophila melanogaster from North America, Europe, and Africa to predict Wolbachia infection status, estimate relative cytoplasmic genome copy number, and reconstruct Wolbachia and mitochondrial genome sequences. Overall, 63% of Drosophila strains were predicted to be infected with Wolbachia by our in silico analysis pipeline, which shows 99% concordance with infection status determined by diagnostic PCR. Complete Wolbachia and mitochondrial genomes show congruent phylogenies, consistent with strict vertical transmission through the maternal cytoplasm and imperfect transmission of Wolbachia. Bayesian phylogenetic analysis reveals that the most recent common ancestor of all Wolbachia and mitochondrial genomes in D. melanogaster dates to around 8,000 years ago. We find evidence for a recent global replacement of ancestral Wolbachia and mtDNA lineages, but our data suggest that the derived wMel lineage arose several thousand years ago, not in the 20th century as previously proposed. Our data also provide evidence that this global replacement event is incomplete and is likely to be one of several similar incomplete replacement events that have occurred since the out-of-Africa migration that allowed D. melanogaster to colonize worldwide habitats. This study provides a complete genomic analysis of the evolutionary mode and temporal dynamics of the D. melanogaster-Wolbachia symbiosis, as well as important resources for further analyses of the impact of Wolbachia on host biology.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003129&type=printable
spellingShingle Mark F Richardson
Lucy A Weinert
John J Welch
Raquel S Linheiro
Michael M Magwire
Francis M Jiggins
Casey M Bergman
Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
PLoS Genetics
title Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
title_full Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
title_fullStr Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
title_full_unstemmed Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
title_short Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster.
title_sort population genomics of the wolbachia endosymbiont in drosophila melanogaster
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003129&type=printable
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