Too “sexy” for the field? Paired measures of laboratory and semi-field performance highlight variability in the apparent mating fitness of Aedes aegypti transgenic strains

Abstract

Background: Evaluating and improving mating success and competitive ability of laboratory-reared transgenic mosquito strains will enhance the effectiveness of proposed disease-control strategies that involve deployment of transgenic strains. Two components of the mosquito rearing process, larval diet quantity and aquatic environment-which are linked to physiological and behavioural differences in adults-are both relatively easy to manipulate. In mosquitoes, as for many other arthropod species, the quality of the juvenile habitat is strongly associated with adult fitness characteristics, such as longevity and fecundity. However, the influence of larval conditioning on mating performance is poorly understood. Here, we investigated the combined effects of larval diet amount and environmental water source on adult male mating success in a genetically modified strain of Aedes aegypti mosquitoes in competition with wild-type conspecifics. Importantly, this research was conducted in a field setting using low generation laboratory and wild-type lines. Results: By controlling larval diet (high and low) and rearing water source (field-collected and laboratory water), we generated four treatment lines of a genetically modified strain of Ae. aegypti tagged with fluorescent sperm. Laboratory reared mosquitoes were then competed against a low generation wild-type colony in a series of laboratory and semi-field mating experiments. While neither food quantity nor larval aquatic environment were found to affect male mating fitness, the transgenic lines consistently outperformed wild-types in laboratory competition assays, an advantage that was not conferred to semi-field tests. Conclusions: Using a model transgenic system, our results indicate that differences in the experimental conditions of laboratory-and field-based measures of mating success can lead to variation in the perceived performance ability of modified strains if they are only tested in certain environments. While there are many potential sources of variation between laboratory and field lines, laboratory adaptation-which may occur over relatively few generations in this species-may directly impact mating ability depending on the context in which it is measured. We suggest that colony-hybridization with field material can potentially be used to mitigate these effects in a field setting. Release programs utilising mass-produced modified laboratory strains should incorporate comparative assessments of quality in candidate lines.

Flight tone characterisation of the South American malaria vector Anopheles darlingi (Diptera: Culicidae)

“…Mosquito mating has been widely used as a target to develop novel control strategies. 42 The effectiveness of such strategies, however, require a profound understanding of behaviors associated with mosquito reproduction, 42 in which flight-tones play a major role. 21 , 43 Increasing our knowledge on the mating behavior of various species provides new insights on different aspects of acoustic interactions that influence mating.…”

Toward the Definition of Efficacy and Safety Criteria for Advancing Gene Drive-Modified Mosquitoes to Field Testing

“…Experiments carried out inside large cages or semifield mesocosms to assess the mating capabilities of transgenic mosquitoes can reveal effects on the fitness/vigor/behavior of SAFETY AND EFFICACY OF GENE DRIVE MOSQUITOES the mosquitoes that are difficult to observe in smaller cages (Facchinelli et al 2013, Aldersley et al 2019. This information could contribute to decision-making about whether or not to advance an investigational gene drive product to field testing.…”

Sexual selection theory meets disease vector control: Testing harmonic convergence as a “good genes” signal inAedes aegyptimosquitoes

“…The Thai mosquitoes used in the present study were derived from wild populations that may have experienced different selective pressures that led to differences in mating behavior compared to the Mexican strains tested in the earlier study. This difference in mating behavior may also stem from the degree to which the strains examined experienced laboratory selection [61–64], as the earlier high generation strain had experienced more generations (roughly 5 years’ worth) of laboratory selective conditions compared to the low generation strain used here. Importantly, while male mating success was assayed under competitive conditions in the previous work, male harmonic convergence and subsequent mating here occurred in one on one interactions, and a recent study in Ae.…”