Wolbachia versus dengue: Evolutionary forecasts
- PMID: 24481199
- PMCID: PMC3847891
- DOI: 10.1093/emph/eot018
Wolbachia versus dengue: Evolutionary forecasts
Abstract
A novel form of biological control is being applied to the dengue virus. The agent is the maternally transmitted bacterium Wolbachia, naturally absent from the main dengue vector, the mosquito Aedes aegypti. Three Wolbachia-based control strategies have been proposed. One is suppression of mosquito populations by large-scale releases of males incompatible with native females; this intervention requires ongoing releases. The other interventions transform wild mosquito populations with Wolbachia that spread via the frequency-dependent fitness advantage of Wolbachia-infected females; those interventions potentially require just a single, local release for area-wide disease control. One of these latter strategies uses Wolbachia that shortens mosquito life, indirectly preventing viral maturation/transmission. The other strategy uses Wolbachia that block viral transmission. All interventions can be undermined by viral, bacterial or mosquito evolution; viral virulence in humans may also evolve. We examine existing theory, experiments and comparative evidence to motivate predictions about evolutionary outcomes. (i) The life-shortening strategy seems the most likely to be thwarted by evolution. (ii) Mosquito suppression has a reasonable chance of working locally, at least in the short term, but long-term success over large areas is challenging. (iii) Dengue blocking faces strong selection for viral resistance but may well persist indefinitely at some level. Virulence evolution is not mathematically predictable, but comparative data provide no precedent for Wolbachia increasing dengue virulence. On balance, our analysis suggests that the considerable possible benefits of these technologies outweigh the known negatives, but the actual risk is largely unknown.
Keywords: biological control; cytoplasmic incompatibility; intervention; population suppression.
Similar articles
-
Deploying dengue-suppressing Wolbachia : Robust models predict slow but effective spatial spread in Aedes aegypti.Theor Popul Biol. 2017 Jun;115:45-60. doi: 10.1016/j.tpb.2017.03.003. Epub 2017 Apr 12. Theor Popul Biol. 2017. PMID: 28411063 Free PMC article.
-
Selection on Aedes aegypti alters Wolbachia-mediated dengue virus blocking and fitness.Nat Microbiol. 2019 Nov;4(11):1832-1839. doi: 10.1038/s41564-019-0533-3. Epub 2019 Aug 26. Nat Microbiol. 2019. PMID: 31451771 Free PMC article.
-
The effect of virus-blocking Wolbachia on male competitiveness of the dengue vector mosquito, Aedes aegypti.PLoS Negl Trop Dis. 2014 Dec 11;8(12):e3294. doi: 10.1371/journal.pntd.0003294. eCollection 2014 Dec. PLoS Negl Trop Dis. 2014. PMID: 25502564 Free PMC article.
-
Wolbachia Biocontrol Strategies for Arboviral Diseases and the Potential Influence of Resident Wolbachia Strains in Mosquitoes.Curr Trop Med Rep. 2016;3:20-25. doi: 10.1007/s40475-016-0066-2. Epub 2016 Feb 2. Curr Trop Med Rep. 2016. PMID: 26925368 Free PMC article. Review.
-
The spread of Wolbachia through mosquito populations.PLoS Biol. 2017 Jun 1;15(6):e2002780. doi: 10.1371/journal.pbio.2002780. eCollection 2017 Jun. PLoS Biol. 2017. PMID: 28570608 Free PMC article. Review.
Cited by
-
Immune-mediated competition benefits protective microbes over pathogens in a novel host species.Heredity (Edinb). 2022 Dec;129(6):327-335. doi: 10.1038/s41437-022-00569-3. Epub 2022 Nov 9. Heredity (Edinb). 2022. PMID: 36352206 Free PMC article.
-
Wolbachia Genome Stability and mtDNA Variants in Aedes aegypti Field Populations Eight Years after Release.iScience. 2020 Sep 16;23(10):101572. doi: 10.1016/j.isci.2020.101572. eCollection 2020 Oct 23. iScience. 2020. PMID: 33083739 Free PMC article.
-
Fitness costs of Wolbachia shift in locally-adapted Aedes aegypti mosquitoes.Environ Microbiol. 2022 Dec;24(12):5749-5759. doi: 10.1111/1462-2920.16235. Epub 2022 Oct 18. Environ Microbiol. 2022. PMID: 36200325 Free PMC article.
-
Genetic stability of Aedes aegypti populations following invasion by wMel Wolbachia.BMC Genomics. 2021 Dec 14;22(1):894. doi: 10.1186/s12864-021-08200-1. BMC Genomics. 2021. PMID: 34906084 Free PMC article.
-
Mutual fitness benefits arise during coevolution in a nematode-defensive microbe model.Evol Lett. 2018 May 28;2(3):246-256. doi: 10.1002/evl3.58. eCollection 2018 Jun. Evol Lett. 2018. PMID: 30283680 Free PMC article.
References
-
- Werren JH. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. - PubMed
-
- Curtis CF, Sinkins SP. Wolbachia as a possible means of driving genes into populations. Parasitology. 1998;116(Suppl):S111–15. - PubMed
-
- Brelsfoard CL, Dobson SL. Short note: an update on the utility of Wolbachia for controlling insect vectors and disease transmission. Aspac J Mol Biol Biotechnol. 2011;19:85–92.
-
- McGraw EA, O’Neill SL. Beyond pesticides: new thinking on an ancient problem. Nat Rev Microbiol. 2013;11:181–93. - PubMed
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources