Does acoustic signalling predict mating success in mosquito lines?

Lead Research Organisation: Imperial College London
Department Name: Life Sciences

Abstract

The control of mosquito transmitted diseases such as malaria, dengue fever, and Chikungunya is still largely dependent on mosquito population control. Unfortunately, many of the tools we use to control mosquito populations are currently threatened by the evolution of insecticide resistance. Researchers are developing new strategies to manage mosquito populations. Several new promising strategies involve genetic or reproductive control. In these cases, males will be mass reared in the laboratory and released into nature where they will need to compete with wild males for mates. These males will deliver technologies that will either reduce the mosquito population or the population's ability to transmit disease. Unfortunately, we know very little about mosquito mating behaviour. Specifically, we do not know what makes a male attractive to females.

In this project, we propose to investigate newly discovered acoustic signals to determine if we can use male signalling ability to accurately predict how laboratory reared males will perform in competition with wild males. So far we know that the presence of a convergence event it important for female choice, but we do not know which components of the signal she is paying attention to. First, we will measure signal components such as latency, rate, range, and consistency while recording mating interactions between live mosquitoes to determine which are most predictive of male mating success. Males used in releases will need to be reared in the laboratory. Thus, understanding how rearing practices influence male courtship signals is important. However, the role of environment in shaping these signals has not been investigated. We will use artificial playbacks to measure the signalling performance of males that have been subjected to various laboratory conditions. Finally, we will use this new knowledge to determine if harmonic convergence signalling ability is a predictor of how males will perform under field conditions. We will test males with low or high signalling performance against wild males in large field cages. This will allow us to test if acoustic measurement could be used as a high-throughput assay to males in rearing programs. At the conclusion of this project, we will have advanced our understanding of sexual selection in mosquitoes and developed a new tool for control programs.

Technical Summary

Mosquito transmitted pathogens represent a substantial and emerging threat to global health. Several new reproductive and genetic control strategies will require the release of laboratory reared male mosquitoes which are able to successfully mate with field populations. However, we know surprisingly little about the determinants of male fitness and mating success. This lack of understanding of basic mosquito ecology has hampered the development of methods for assessing line quality. We have published evidence that mosquitoes use acoustic signals and that these signals are significant determinants of male mating success. In this application we will investigate the role of acoustic signalling in mate choice and assess the utility of acoustic signals as an indicator of male mosquito fitness. In order to meet the applied goals of rearing successful lines and developing robust, accurate methods for predicting male fitness, we must first better understand how environmental conditions affect acoustic signals and the relative contribution of acoustic signalling to total male fitness. First, we will measure signal components, such as latency and speed, while recording mating interactions between live mosquitoes to determine which are most predictive of male mating success. Second, we will use artificial playbacks to measure the signalling performance of males that have been subjected to various laboratory rearing conditions. Finally, we will use this new knowledge to determine if acoustic signalling ability is a predictor of how males will perform under field conditions. We will test males with low or high signalling performance against wild males in large field cages. This will allow us to test if high-throughput acoustic assays can be used to assess males in rearing programs. At the conclusion of this project, we will have advanced our understanding of mosquito sexual selection and aim to provide a new tool for mass rearing programs to assess mosquito line quality.

Planned Impact

This research would benefit:
The commercial private sector and non-for-profit control projects would benefit from the development of a high throughput assay for assessing mosquito lines. The ability to test and optimized lines would be helpful for the design of large scale rearing production centers and would assist these parties in increasing the effectiveness and economic feasibility of large scale releases. We will provide these parties with key data on potential high-throughput assays for assess line quality and how rearing conditions affect male performance in competition with wild males. We are working closely with industry partners (see letters of support from Oxitech and Target Malaria). Project PI Cator is in active communication with these parties and will ensure thatresults of the project are made available to them directly and to the wider community through presentations and publications.

The wider public will benefit from this research because it will facilitate with implementation of novel control strategies for diseases that continue to be significant sources of death and suffering throughout much of the world. Additionally, this project will contribute to the UK's competitiveness in this area by training project staff in techniques and forging collaborations between UK academics, industry, and international partners.

Publications

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Andrés M (2020) Buzzkill: targeting the mosquito auditory system. in Current opinion in insect science

 
Description We have developed new techniques for observing mosquito mating and recording duets between males and females in flight. We have found additional evidence to support the hypothesis that females are using male acoustic signals to decide which males to mate with. We also clarified the relationships between different signal components and mating behaviour using slow motion videography.

Laboratory experiments indicated that feeding males more as larvae does not improve their ability to produce these signals or the likelihood that a given female will mate with them, it does look like it increases their opportunities for mating by increasing their survival and how long they can participate in a mating swarm. We tested these diets in large field cages in Thailand and found that feeding males different amount did not have an effect on their mating success in competition with wild type males.

Additionally, we recently completed a long term experiment investigating the effects of adult sex ratios during mating on colony fitness and the potential for evolved variation in male mating success from these conditions. Our results indicate that males that are held in high competition mating environments are more likely to achieve mating in competition with unselected males. The idea that there is rapid selection in these phenotypes was reflected in our fieldwork data. Even low generation laboratory males (<5 generations in lab) exhibited higher mating success under lab conditions compared to males from field populations. This apparent advantage disappeared in large semi-field conditions. This data suggest that the laboratory environment likely selects on male mating phenotypes and that we may be able to maximize male mating success by altering selective conditions more efficiently than say increasing diet.
Exploitation Route Future rearing and new control designs in particular methods for mitigating the negative effects of laboratory adaptation.
Sectors Environment

URL https://www.ncbi.nlm.nih.gov/pubmed/27906074
 
Description Our findings support on going control of Aedes mosquitoes using SIT and is currently being applied to inform mass-rearing operations.
First Year Of Impact 2022
Sector Other
Impact Types Policy & public services

 
Description Genomic signatures of sexual selection in the Yellow Fever mosquito.
Amount £15,000 (GBP)
Funding ID 2286561 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2019 
End 05/2023
 
Description Bugs 2018 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Bugs Day is an Open Day at Silwood Park. Lab members run a booth on mosquito biology with live specimens and educations displays on the mosquito life cycle. Children are invited to "build" their own mosquito to take home with them.
Year(s) Of Engagement Activity 2016,2017,2018,2019
 
Description Bugs Day 2016! 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Cator lab members put on a "Build a Mosquito!" booth at campus open day. The activity was aimed at primary ages school children. We taugh basic mosquito anatomy and biology.
Year(s) Of Engagement Activity 2016
URL http://www3.imperial.ac.uk/newsandeventspggrp/imperialcollege/administration/outreach/eventssummary/...
 
Description Outreach 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Silwood Open Day- Ran an exhibit on VBDs in the UK (covering both mosquitoes and ticks). Approximately 300 members of the public attended. Many good questions about controlling mosquitoes in your own backyard.
Year(s) Of Engagement Activity 2019
URL http://www3.imperial.ac.uk/newsandeventspggrp/imperialcollege/eventssummary/event_3-7-2019-12-7-49
 
Description Outreach- Imperial Festival 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Participated in Imperial College's Festival. This event attracts thousands of visitors to the South Kensington Campus. We rana day long demonstration on mosquito mating behavior and acoustic biology. Many visitors from all over the world asked questions and discussion ranged from personal protection measures to the implications of GM technologies.
Year(s) Of Engagement Activity 2019
URL https://www.imperial.ac.uk/news/191766/first-ever-great-exhibition-road-festival/
 
Description Pint of Science 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Dr. Cator gave a presentation on the importance of mosquito ecology for understanding and controlling mosquito transmitted diseases as part of the international "Pint of Science" festival.
Year(s) Of Engagement Activity 2016
URL https://pintofscience.co.uk/