Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies

Abstract Background The endosymbiotic relationship between Wolbachia bacteria and insects has been of interest for many years due to their diverse types of host reproductive phenotypic manipulation and potential role in the host’s evolutionary history and population dynamics. Even though infection r...

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Main Authors: Pedro Ribeiro, Anzhelika Butenko, Daniel Linke, Hamid Reza Ghanavi, Joana Isabel Meier, Niklas Wahlberg, Pável Matos-Maraví
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Microbiology
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Online Access:https://doi.org/10.1186/s12866-024-03719-1
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author Pedro Ribeiro
Anzhelika Butenko
Daniel Linke
Hamid Reza Ghanavi
Joana Isabel Meier
Niklas Wahlberg
Pável Matos-Maraví
author_facet Pedro Ribeiro
Anzhelika Butenko
Daniel Linke
Hamid Reza Ghanavi
Joana Isabel Meier
Niklas Wahlberg
Pável Matos-Maraví
author_sort Pedro Ribeiro
collection DOAJ
description Abstract Background The endosymbiotic relationship between Wolbachia bacteria and insects has been of interest for many years due to their diverse types of host reproductive phenotypic manipulation and potential role in the host’s evolutionary history and population dynamics. Even though infection rates are high in Lepidoptera and specifically in butterflies, and reproductive manipulation is present in these taxa, less attention has been given to understanding how Wolbachia is acquired and maintained in their natural populations, across and within species having continental geographical distributions. Results We used whole genome sequencing data to investigate the phylogenetics, demographic history, and infection rate dynamics of Wolbachia in four species of the Spicauda genus of skipper butterflies (Lepidoptera: Hesperiidae), a taxon that presents sympatric and often syntopic distribution, with drastic variability in species abundance in the Neotropical region. We show that infection is maintained by high turnover rates driven mainly by pervasive horizontal transmissions, while also presenting novel cases of double infection by distantly related supergroups of Wolbachia in S. simplicius. Conclusions Our results suggest that Wolbachia population dynamics is host species-specific, with genetic cohesiveness across wide geographical distributions. We demonstrate that low coverage whole genome sequencing data can be used for an exhaustive assessment of Wolbachia infection in natural populations of butterflies, as well as its dynamics in closely related host species. This ultimately leads to a better understanding of the endosymbiotic population dynamics of Wolbachia and its effects on the host’s biology and evolution.
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issn 1471-2180
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spelling doaj-art-04baf7a2e76646c89d26a1855c5ca3282025-01-12T12:10:06ZengBMCBMC Microbiology1471-21802025-01-0125111310.1186/s12866-024-03719-1Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterfliesPedro Ribeiro0Anzhelika Butenko1Daniel Linke2Hamid Reza Ghanavi3Joana Isabel Meier4Niklas Wahlberg5Pável Matos-Maraví6Biology Centre of the Czech Academy of Sciences, Institute of EntomologyFaculty of Science, University of South BohemiaBiology Centre of the Czech Academy of Sciences, Institute of EntomologyFunctional Zoology Unit, Department of Biology, Lund UniversityDepartment of Zoology, University of CambridgeBiodiversity Unit, Department of Biology, Lund UniversityBiology Centre of the Czech Academy of Sciences, Institute of EntomologyAbstract Background The endosymbiotic relationship between Wolbachia bacteria and insects has been of interest for many years due to their diverse types of host reproductive phenotypic manipulation and potential role in the host’s evolutionary history and population dynamics. Even though infection rates are high in Lepidoptera and specifically in butterflies, and reproductive manipulation is present in these taxa, less attention has been given to understanding how Wolbachia is acquired and maintained in their natural populations, across and within species having continental geographical distributions. Results We used whole genome sequencing data to investigate the phylogenetics, demographic history, and infection rate dynamics of Wolbachia in four species of the Spicauda genus of skipper butterflies (Lepidoptera: Hesperiidae), a taxon that presents sympatric and often syntopic distribution, with drastic variability in species abundance in the Neotropical region. We show that infection is maintained by high turnover rates driven mainly by pervasive horizontal transmissions, while also presenting novel cases of double infection by distantly related supergroups of Wolbachia in S. simplicius. Conclusions Our results suggest that Wolbachia population dynamics is host species-specific, with genetic cohesiveness across wide geographical distributions. We demonstrate that low coverage whole genome sequencing data can be used for an exhaustive assessment of Wolbachia infection in natural populations of butterflies, as well as its dynamics in closely related host species. This ultimately leads to a better understanding of the endosymbiotic population dynamics of Wolbachia and its effects on the host’s biology and evolution.https://doi.org/10.1186/s12866-024-03719-1HesperiidaeWolbachiaPhylogeneticsPopulation dynamicsHistorical demographySkipper butterflies
spellingShingle Pedro Ribeiro
Anzhelika Butenko
Daniel Linke
Hamid Reza Ghanavi
Joana Isabel Meier
Niklas Wahlberg
Pável Matos-Maraví
Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
BMC Microbiology
Hesperiidae
Wolbachia
Phylogenetics
Population dynamics
Historical demography
Skipper butterflies
title Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
title_full Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
title_fullStr Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
title_full_unstemmed Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
title_short Pervasive horizontal transmission of Wolbachia in natural populations of closely related and widespread tropical skipper butterflies
title_sort pervasive horizontal transmission of wolbachia in natural populations of closely related and widespread tropical skipper butterflies
topic Hesperiidae
Wolbachia
Phylogenetics
Population dynamics
Historical demography
Skipper butterflies
url https://doi.org/10.1186/s12866-024-03719-1
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