Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

Lee, Chih-Chi; Lin, Chun-Yi; Tseng, Shiojenn; Matsuura, Kenji; Yang, Chun‐Pai

doi:10.3390/microorganisms8101569

Cited by 13 publications

(14 citation statements)

References 81 publications

(108 reference statements)

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“…Similar infection patterns have been found in the invasive yellow crazy ant Anoplolepis gracilipes (Lee et al. 2020). In contrast, Wolbachia infection is facultative in the closely related invasive ant Monomorium pharaonis (Pontieri et al.…”

Section: Discussionsupporting

confidence: 83%

“…Wolbachia clearly play a significant role in the biology of the ant host, with all screened individuals infected regardless of population, caste, or sex. Similar infection patterns have been found in the invasive yellow crazy ant Anoplolepis gracilipes (Lee et al 2020). In contrast, Wolbachia infection is facultative in the closely related invasive ant Monomorium pharaonis (Pontieri et al 2017).…”

Section: Discussionsupporting

confidence: 72%

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Cytoplasmic incompatibility between Old and New World populations of a tramp ant

et al. 2021

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Reproductive manipulation by endosymbioticWolbachia can cause unequal inheritance, allowing the manipulator to spread and potentially impacting evolutionary dynamics in infected hosts. Tramp and invasive species are excellent models to study the dynamics of host-Wolbachia associations because introduced populations often diverge in their microbiomes after colonizing new habitats, resulting in infection polymorphisms between native and introduced populations. Ants are the most abundant group of insects on earth, and numerous ant species are classified as highly invasive. However, little is known about the role of Wolbachia in these ecologically dominant insects. Here, we provide the first description of reproductive manipulation by Wolbachia in an ant. We show that Old and New World populations of the cosmotropic tramp ant Cardiocondyla obscurior harbor distinct Wolbachia strains, and that only the Old World strain manipulates host reproduction by causing cytoplasmic incompatibility (CI) in hybrid crosses. By uncovering a symbiont-induced mechanism of reproductive isolation in a social insect, our study provides a novel perspective on the biology of tramp ants and introduces a new system for studying the evolutionary consequences of CI.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionsupporting

confidence: 72%

Cytoplasmic incompatibility between Old and New World populations of a tramp ant

et al. 2021

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“…stephensi populations. As an endosymbiont of invasive mosquitoes, the Wolbachia population should mirror a lower level of diversity in its invasive host population relative to the corresponding host source population [ 43 , 44 ]. A study in pre-print from the state of Tamil Nadu, India, detected four haplotypes of Wolbachia 16S , and in eastern Ethiopia we detected three haplotypes.…”

Section: Discussionmentioning

confidence: 99%

Wolbachia 16S rRNA haplotypes detected in wild Anopheles stephensi in eastern Ethiopia

et al. 2022

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Background About two out of three Ethiopians are at risk of malaria, a disease caused by the parasites Plasmodium falciparum and Plasmodium vivax. Anopheles stephensi, an invasive vector typically found in South Asia and the Middle East, was recently found to be distributed across eastern and central Ethiopia and is capable of transmitting both P. falciparum and P. vivax. The detection of this vector in the Horn of Africa (HOA) coupled with widespread insecticide resistance requires that new methods of vector control be investigated in order to control the spread of malaria. Wolbachia, a naturally occurring endosymbiotic bacterium of mosquitoes, has been identified as a potential vector control tool that can be explored for the control of malaria transmission. Wolbachia could be used to control the mosquito population through suppression or potentially decrease malaria transmission through population replacement. However, the presence of Wolbachia in wild An. stephensi in eastern Ethiopia is unknown. This study aimed to identify the presence and diversity of Wolbachia in An. stephensi across eastern Ethiopia. Methods DNA was extracted from An. stephensi collected from eastern Ethiopia in 2018 and screened for Wolbachia using a 16S targeted PCR assay, as well as multilocus strain typing (MLST) PCR assays. Haplotype and phylogenetic analysis of the sequenced 16S amplicons were conducted to compare with Wolbachia from countries across Africa and Asia. Results Twenty out of the 184 mosquitoes screened were positive for Wolbachia, with multiple haplotypes detected. In addition, phylogenetic analysis revealed two superclades, representing Wolbachia supergroups A and B (bootstrap values of 81 and 72, respectively) with no significant grouping of geographic location or species. A subclade with a bootstrap value of 89 separates the Ethiopian haplotype 2 from other sequences in that superclade. Conclusions These findings provide the first evidence of natural Wolbachia populations in wild An. stephensi in the HOA. They also identify the need for further research to confirm the endosymbiotic relationship between Wolbachia and An. stephensi and to investigate its utility for malaria control in the HOA. Graphical Abstract

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“…The yellow crazy ant, Anoplolepis gracilipes , is a globally distributed invasive ant; yet, the native range of this ant species remains debatable as multiple datasets failed to reach consensus [ 13 ]. However, new lines of evidence have been recently accumulated to support the Southeast Asian origin of this ant [ 14 , 15 , 16 ]. High enemy/pathogen diversities and loads may indicate an invasive species’ native range as invasion likely filters out certain enemies/pathogens due to invading propagules representing only a small proportion of the native or source population [ 17 ].…”

Section: Introductionmentioning

confidence: 99%

First Polycipivirus and Unmapped RNA Virus Diversity in the Yellow Crazy Ant, Anoplolepis gracilipes

Lee

Hsu

Lin

et al. 2022

Viruses

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The yellow crazy ant, Anoplolepis gracilipes is a widespread invasive ant that poses significant threats to local biodiversity. Yet, compared to other global invasive ant species such as the red imported fire ant (Solenopsis invicta) or the Argentine ant (Linepithema humile), little is known about the diversity of RNA viruses in the yellow crazy ant. In the current study, we generated a transcriptomic database for A. gracilipes using a high throughput sequencing approach to identify new RNA viruses and characterize their genomes. Four virus species assigned to Dicistroviridae, two to Iflaviridae, one to Polycipiviridae, and two unclassified Riboviria viruses were identified. Detailed genomic characterization was carried out on the polycipivirus and revealed that this virus comprises 11,644 nucleotides with six open reading frames. Phylogenetic analysis and pairwise amino acid identity comparison classified this virus into the genus Sopolycivirus under Polycipiviridae, which is tentatively named “Anoplolepis gracilipes virus 3 (AgrV-3)”. Evolutionary analysis showed that AgrV-3 possesses a high level of genetic diversity and elevated mutation rate, combined with the common presence of multiple viral strains within single worker individuals, suggesting AgrV-3 likely evolves following the quasispecies model. A subsequent field survey placed the viral pathogen “hotspot” of A. gracilipes in the Southeast Asian region, a pattern consistent with the region being recognized as part of the ant’s native range. Lastly, infection of multiple virus species seems prevalent across field colonies and may have been linked to the ant’s social organization.

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Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

Cited by 13 publications

References 81 publications

Cytoplasmic incompatibility between Old and New World populations of a tramp ant

Cytoplasmic incompatibility between Old and New World populations of a tramp ant

Wolbachia 16S rRNA haplotypes detected in wild Anopheles stephensi in eastern Ethiopia

First Polycipivirus and Unmapped RNA Virus Diversity in the Yellow Crazy Ant, Anoplolepis gracilipes

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