Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts
Wolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis...
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doaj-9b31743dc49f4df7bfa7b0023e00dd6c2020-11-24T23:19:47ZengPeerJ Inc.PeerJ2167-83592016-03-014e184010.7717/peerj.1840Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hostsEmilie Lefoulon0Odile Bain1Benjamin L. Makepeace2Cyrille d’Haese3Shigehiko Uni4Coralie Martin5Laurent Gavotte6UMR7245, MCAM, Museum national d’Histoire naturelle, Paris, FranceUMR7245, MCAM, Museum national d’Histoire naturelle, Paris, FranceInstitute of Infection and Global Health, University of Liverpool, Liverpool, United KingdomUMR7179 MECADEV, Museum national d’Histoire naturelle, Paris, FranceInstitute of Biological Sciences, University of Malaya, Kuala Lumpur, MalaysiaUMR7245, MCAM, Museum national d’Histoire naturelle, Paris, FranceUMR5554 ISEM, Université de Montpellier II, Montpellier, FranceWolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from the Wolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures in Wolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae and Wolbachia has been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquired Wolbachia. Here, we present the largest co-phylogenetic analysis of Wolbachia in filariae performed to date including: (i) a screening and an updated phylogeny of Wolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition of Wolbachia infection. First, our results show a general overestimation of Wolbachia occurrence and support the hypothesis of an ancestral absence of infection in the nematode phylum. The accuracy of supergroup J is also underlined. Second, although a global pattern of coevolution remains, the signal is derived predominantly from filarial clades associated with Wolbachia in supergroups C and J. In other filarial clades, harbouring Wolbachia supergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basal Wolbachia clade within the Ecdysozoa. This hypothesis on the origin of Wolbachia would change drastically our understanding of Wolbachia evolution.https://peerj.com/articles/1840.pdfSymbiosisHorizontal transmissionCophylogenetic analysisWolbachiaCoevolution Filarial nematodes |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Emilie Lefoulon Odile Bain Benjamin L. Makepeace Cyrille d’Haese Shigehiko Uni Coralie Martin Laurent Gavotte |
spellingShingle |
Emilie Lefoulon Odile Bain Benjamin L. Makepeace Cyrille d’Haese Shigehiko Uni Coralie Martin Laurent Gavotte Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts PeerJ Symbiosis Horizontal transmission Cophylogenetic analysis Wolbachia Coevolution Filarial nematodes |
author_facet |
Emilie Lefoulon Odile Bain Benjamin L. Makepeace Cyrille d’Haese Shigehiko Uni Coralie Martin Laurent Gavotte |
author_sort |
Emilie Lefoulon |
title |
Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts |
title_short |
Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts |
title_full |
Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts |
title_fullStr |
Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts |
title_full_unstemmed |
Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts |
title_sort |
breakdown of coevolution between symbiotic bacteria wolbachia and their filarial hosts |
publisher |
PeerJ Inc. |
series |
PeerJ |
issn |
2167-8359 |
publishDate |
2016-03-01 |
description |
Wolbachia is an alpha-proteobacterial symbiont widely distributed in arthropods. Since the identification of Wolbachia in certain animal-parasitic nematodes (the Onchocercidae or filariae), the relationship between arthropod and nematode Wolbachia has attracted great interest. The obligate symbiosis in filariae, which renders infected species susceptible to antibiotic chemotherapy, was held to be distinct from the Wolbachia-arthropod relationship, typified by reproductive parasitism. While co-evolutionary signatures in Wolbachia-arthropod symbioses are generally weak, reflecting horizontal transmission events, strict co-evolution between filariae and Wolbachia has been reported previously. However, the absence of close outgroups for phylogenetic studies prevented the determination of which host group originally acquired Wolbachia. Here, we present the largest co-phylogenetic analysis of Wolbachia in filariae performed to date including: (i) a screening and an updated phylogeny of Wolbachia; (ii) a co-phylogenetic analysis; and (iii) a hypothesis on the acquisition of Wolbachia infection. First, our results show a general overestimation of Wolbachia occurrence and support the hypothesis of an ancestral absence of infection in the nematode phylum. The accuracy of supergroup J is also underlined. Second, although a global pattern of coevolution remains, the signal is derived predominantly from filarial clades associated with Wolbachia in supergroups C and J. In other filarial clades, harbouring Wolbachia supergroups D and F, horizontal acquisitions and secondary losses are common. Finally, our results suggest that supergroup C is the basal Wolbachia clade within the Ecdysozoa. This hypothesis on the origin of Wolbachia would change drastically our understanding of Wolbachia evolution. |
topic |
Symbiosis Horizontal transmission Cophylogenetic analysis Wolbachia Coevolution Filarial nematodes |
url |
https://peerj.com/articles/1840.pdf |
work_keys_str_mv |
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