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      Heatwaves cause fluctuations in wMel Wolbachia densities and frequencies in Aedes aegypti

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          Abstract

          Aedes aegypti mosquitoes infected with the wMel strain of Wolbachia are being released into natural mosquito populations in the tropics as a way of reducing dengue transmission. High temperatures adversely affect wMel, reducing Wolbachia density and cytoplasmic incompatibility in some larval habitats that experience large temperature fluctuations. We monitored the impact of a 43.6°C heatwave on the wMel infection in a natural population in Cairns, Australia, where wMel was first released in 2011 and has persisted at a high frequency. Wolbachia infection frequencies in the month following the heatwave were reduced to 83% in larvae sampled directly from field habitats and 88% in eggs collected from ovitraps, but recovered to be near 100% four months later. Effects of the heatwave on wMel appeared to be stage-specific and delayed, with reduced frequencies and densities in field-collected larvae and adults reared from ovitraps but higher frequencies in field-collected adults. Laboratory experiments showed that the effects of heatwaves on cytoplasmic incompatibility and density are life stage-specific, with first instar larvae being the most vulnerable to temperature effects. Our results indicate that heatwaves in wMel-infected populations will have only temporary effects on Wolbachia frequencies and density once the infection has established in the population. Our results are relevant to ongoing releases of wMel-infected Ae. aegypti in several tropical countries.

          Author summary

          Mosquitoes infected with Wolbachia bacteria are being released in the tropics to replace natural mosquito populations and suppress dengue transmission. Aedes aegypti mosquitoes with the wMel strain of Wolbachia were first released in Cairns, Australia in 2011 and releases were then expanded to the entire city and surrounding suburbs. Today, wMel is at a high frequency within the Ae. aegypti population and local dengue transmission in Cairns has declined to nearly zero. Wolbachia infections are vulnerable to high temperatures and the ability of wMel to persist in populations and block dengue may be constrained by climate. Cairns experienced a record heatwave of 43.6°C in November 2018 and we wanted to see whether this affected the wMel-infected Ae. aegypti population. Our results show that the frequency and density of wMel declined after the heatwave, with effects depending on the mosquito life stage tested. When we monitored the population again in April 2019, wMel had returned to a high frequency. We suggest that heatwaves of the magnitude experienced in Cairns will not have long-term impacts on the wMel infection but may affect invasion during releases or interfere with dengue blockage. Heatwaves may affect interventions with wMel-infected Ae. aegypti that are being deployed in several countries. Effects may depend on the proportion of larval habitats that are protected from extreme temperature fluctuations.

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          Updated analyses of temperature and precipitation extreme indices since the beginning of the twentieth century: The HadEX2 dataset

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            Incompatible and sterile insect techniques combined eliminate mosquitoes

            The radiation-based sterile insect technique (SIT) has successfully suppressed field populations of several insect pest species, but its effect on mosquito vector control has been limited. The related incompatible insect technique (IIT)-which uses sterilization caused by the maternally inherited endosymbiotic bacteria Wolbachia-is a promising alternative, but can be undermined by accidental release of females infected with the same Wolbachia strain as the released males. Here we show that combining incompatible and sterile insect techniques (IIT-SIT) enables near elimination of field populations of the world's most invasive mosquito species, Aedes albopictus. Millions of factory-reared adult males with an artificial triple-Wolbachia infection were released, with prior pupal irradiation of the released mosquitoes to prevent unintentionally released triply infected females from successfully reproducing in the field. This successful field trial demonstrates the feasibility of area-wide application of combined IIT-SIT for mosquito vector control.
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              Harnessing mosquito-Wolbachia symbiosis for vector and disease control.

              Mosquito species, members of the genera Aedes, Anopheles and Culex, are the major vectors of human pathogens including protozoa (Plasmodium sp.), filariae and of a variety of viruses (causing dengue, chikungunya, yellow fever, West Nile). There is lack of efficient methods and tools to treat many of the diseases caused by these major human pathogens, since no efficient vaccines or drugs are available; even in malaria where insecticide use and drug therapies have reduced incidence, 219 million cases still occurred in 2010. Therefore efforts are currently focused on the control of vector populations. Insecticides alone are insufficient to control mosquito populations since reduced susceptibility and even resistance is being observed more and more frequently. There is also increased concern about the toxic effects of insecticides on non-target (even beneficial) insect populations, on humans and the environment. During recent years, the role of symbionts in the biology, ecology and evolution of insect species has been well-documented and has led to suggestions that they could potentially be used as tools to control pests and therefore diseases. Wolbachia is perhaps the most renowned insect symbiont, mainly due to its ability to manipulate insect reproduction and to interfere with major human pathogens thus providing new avenues for pest control. We herein present recent achievements in the field of mosquito-Wolbachia symbiosis with an emphasis on Aedes albopictus. We also discuss how Wolbachia symbiosis can be harnessed for vector control as well as the potential to combine the sterile insect technique and Wolbachia-based approaches for the enhancement of population suppression programs. Copyright © 2013 International Atomic Energy Agency 2013. Published by Elsevier B.V. All rights reserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                23 January 2020
                January 2020
                : 14
                : 1
                : e0007958
                Affiliations
                [1 ] Pest and Environmental Adaptation Research Group, Bio21 Institute and the School of BioSciences, The University of Melbourne, Parkville, Victoria, Australia
                [2 ] College of Public Health, Medical and Veterinary Sciences, James Cook University, Smithfield, Queensland, Australia
                [3 ] Australian Institute of Tropical Health and Medicine, James Cook University, Smithfield, Queensland, Australia
                University of Glasgow, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-7645-7523
                Article
                PNTD-D-19-01580
                10.1371/journal.pntd.0007958
                6977724
                31971938
                82ca2ce5-59b9-44b6-9e41-41d23e01f247
                © 2020 Ross et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 September 2019
                : 27 November 2019
                Page count
                Figures: 7, Tables: 1, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: 1132412
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000925, National Health and Medical Research Council;
                Award ID: 1118640
                Award Recipient :
                AAH was supported by the National Health and Medical Research Council (1132412, 1118640, www.nhmrc.gov.au). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Bacteria
                Wolbachia
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Pupae
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Population Density
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Light
                Sunlight
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Solar Radiation
                Sunlight
                People and Places
                Geographical Locations
                Oceania
                Australia
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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