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...
Saved in:
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2025-01-01
|
Series: | BMC Microbiology |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12866-024-03719-1 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1841544916954513408 |
---|---|
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. |
format | Article |
id | doaj-art-04baf7a2e76646c89d26a1855c5ca328 |
institution | Kabale University |
issn | 1471-2180 |
language | English |
publishDate | 2025-01-01 |
publisher | BMC |
record_format | Article |
series | BMC Microbiology |
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 |
work_keys_str_mv | AT pedroribeiro pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT anzhelikabutenko pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT daniellinke pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT hamidrezaghanavi pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT joanaisabelmeier pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT niklaswahlberg pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies AT pavelmatosmaravi pervasivehorizontaltransmissionofwolbachiainnaturalpopulationsofcloselyrelatedandwidespreadtropicalskipperbutterflies |