The challenge of measuring mosquito flight performance: going beyond sterile insect technique and into transgenic and gene drive-based approaches

Abstract

Invasive insects inflict global costs of more than 70 billion USD annually by destroying crops and spreading disease-causing pathogens. Sterile insect technique (SIT), an insect population control method, involves the irradiation or chemical sterilization of insects to produce sterile males that are mass-released. SIT has proven effective in reducing populations of the Mediterranean fruit fly, Mexican fruit fly and screwworm fly. In the past decade, efforts to improve SIT with transgenic approaches have increased, including the development of potentially highly invasive gene drive transgenes. Determining flight capability is vital to the success of any insect control programme, and various flight assays can be used to analyse insect dispersal, flight behaviour and the mechanics behind flight. However, traditional flight assays such as mark-release-recapture become more challenging with transgenic or gene drive arthropods due to ecological concerns, while assays such as wind tunnels or flight mills/arenas may not capture the full range of flight abilities. This review seeks to cover current flight assays and their limitations as well as the requirements for flight assays to establish comparative flight ability for genetically modified insects to better prioritize strains prior to any potential field-based releases.

Keywords: flight assays; gene drive; mark–release–recapture; sterile insect technique.

Figure 1.

Tethered flight assays. Static tethers hold the insect, so the insect flies in place. The insect can rotate (in terms of pitch, yaw or roll) which can be measured using high-speed cameras. Flight mills use tethers to fix the insect to the mill. The insect can fly on a restricted flight path. Flight mills can measure velocity, distance flown and periodicity (the number of flight bouts initiated in a period of time). In both types of flight assays, the insect does not have to produce thrust since it is suspended in the air. Thus, results must be corrected for drag and lift.

Figure 2.

Wind tunnel. Wind tunnels are a commonly used behavioural assay used for olfactory and/or flight studies. The basic design of wind tunnels uses a tunnel where the insects are released, a fan to produce wind, mesh to provide laminar flow and a cue to induce flight in the insects. Wind tunnels can measure velocity, flight distance, flight duration and periodicity. They are often used in olfactory studies to observe flight behaviour in response to semiochemicals.

Figure 3.

Flight arena. Typically cubes, flight arenas allow for free flight, which is tracked using video cameras. A cue is needed to induce flight. Flight arenas can be used to measure flight distance, duration, velocity and periodicity.

Figure 4.

Other flight testers. (a) D. melanogaster are dropped into the metre-high flight column where they fall freely. The flies recover from falling and land at varying heights of the column. Based on their landing position, the flies are categorized as weak, moderate or strong fliers. Flies that could not recover fall into mineral oil at the bottom of the column. (b) The flight test device (FTD) was designed to evaluate the flight performance of mosquitoes before mass-release for insect control programmes. Mosquitoes are placed into the FTD, where they must fly up and escape through one of the flight tubes. Successful mosquitoes can be collected from the larger containment tube. (c) The induced flight activity test (INFLATE) quantifies flight activity in mosquitoes. The cage is tapped on a benchtop to gather the mosquitoes on the bottom of the cage. After 1 min, the mosquitoes are scored based on their position in the cage, with a score of zero assigned to the mosquitoes still on the bottom of the cage. The flight cage is divided into four quadrants with scores ranging from one to four as height increases.