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Understanding sexual selection to help controlling an invasive pest species

Periodic Reporting for period 1 - SexSelec_Invasion (Understanding sexual selection to help controlling an invasive pest species)

Periodo di rendicontazione: 2018-03-01 al 2020-02-29

Understanding the operation of sexual selection is particularly relevant in pest insect species, where mating strategies can be exploited to control populations. Sterile Insect Techniques (SITs) consist of frequent releases of a high number of mass-reared sterile males to induce sterile matings. These techniques have been prioritised because of their limited side-effects on the ecosystem. Unfortunately, SITs run the risk of female counter-adaptation if female choice evolves to discriminate against released males. Drosophila suzukii, the ‘spotted-wing drosophila’ is a champion of invasion that colonised several continents and islands in the last two decades. Because D. suzukii feeds and oviposits on close-to-be-marketed fruits, it causes considerable economic losses. The situation requires rapid development of sustainable, affordable, and environment friendly methods to control D. suzukii.

The results of this project provide a fundamental understanding of how male sexual traits and female preference for those traits co-evolve; essential information for the development of sustainable, environment friendly methods to fight pest species. I have combined cutting-edge techniques spanning behavioural ecology, large-scale phenotyping, and quantitative genetic tools to target three aims:

• Identify male traits that predict male mating success, to mass-produce sterile males that are competitive with local males to mate with local females. Shape, size, and darkness of male wing spots best predicted their mating success.

• Understand the genetic architecture of male sexual traits, to know the relative contributions of genetic factors and environmental conditions in order to optimize the production of attractive sterile males. Results suggest that male attractive wing spot is largely due their genetic background.

• Determine whether females can counter-adapt to SITs by discriminating against sterile males. After using divergent artificial selection towards high and low values of the male wing spot attractiveness, I observed no evolution of female choice evolution, suggesting that female choice would not rapidly counter-adapt to SITs.
I performed an extensive mating assay in Drosophila suzukii and compared numerous male traits in more than 1000 successful and unsuccessful males. Analysed traits included body size, wing size, wing shape, male wing spot’s size, shape and colour, ‘wing-interference patterns’ (WIPs), a structural colour pattern observed in fly and wasp wings, fat contents, and contact pheromones, the Cuticular HydroCarbons (CHCs). Data analysis revealed that size, shape, and darkness of male wing spots best predicted male mating success in D. suzukii.
• Male wing spot traits are good predictors of mating success

Further, we estimated the genetic contributions in those wing traits by measuring them in a structured population (199 fathers and 999 sons). Most studied traits were strongly impacted by genetic factors. In particular, the combination of wing-spot traits that predicted male mating success had a heritability H2 = 0.49 so that around half of the variance in wing-spot male attractiveness is due to genetic factors.
• Male wing spot traits are heritable

Finally, a 7 generations experimental evolution created divergent artificial selection to select males with high, and low values of the wing-spot traits that predicted mating success. Further, the opportunity for sexual selection was maintained in half of the lines whilst random matings were enforced in the other lines. I then measured whether female mate choice had changed depending on the selection operating on male traits. I am currently analysing the vast data collected during this experiment. Preliminary results suggest that female choice was not affected by the selection on male traits, limiting their ability to counter-adapt SITs.
• Female choice does not rapidly evolve to selection on male traits

Because of the delay incurred from an improvement in the design of the first Work Package, and because all further work packages depend on the first publication, there are no scientific publications accepted at this time. Results have been disseminated in the scientific community through conferences and via regular social media updates. Importantly, preliminary results were shared to a wide audience of French agriculture and science stakeholders during the “Journée nationale Drosophila suzukii” and to an international research network aiming at developing SIT on this emerging pest (March 2019, Mendoza, Argentina).
This project enabled to shed an unprecedented light to the evolutionary processes leading to the evolution of male extravagant sexual traits and female preference for those by (i) understanding the relative importance and the combined function of numerous male traits to their mating success (ii) showing the maintenance of genetic variation in male traits despite being sexually selected, (iii) elucidating the co-evolution of female preference and male traits, and (iv) describing functional trade-offs between male sexual traits and other components of male fitness.

This project significantly contributed to the researcher’s career and her collaborators and students. The researcher trained in several techniques thanks to the collaboration network she set up. She learned how to use machine learning tools to describe Drosophila wings at the pixel level and performed large-scale experimental evolution. This fellowship, its prestige and scientific outcomes, has enabled the researcher to increase her competitiveness to reach an independent research position, showing her scientific maturity and ability to lead a project. It has also broadened the scope of the researcher’s intended audience with interactions with agronomic scientists, the biochemistry industry, farmers, and policymakers. This project also contributed to the researcher’s skill to lead her own group, as it was her first experience to fully mentor a successful postgraduate student, who since enrolled in the PhD program of her choice.

Importantly, this series of results will help design SITs in D. suzukii and in other species (i) identifying attractive male traits to produce high quality sterile males that can compete with wild males (ii) understanding the genetic architecture of those traits to design optimal genetic and environmental conditions for male mass-production (iii) ensuring the absence or very slow counter-adaptation of female choice. Altogether, this project is a promising proof-of-evidence that SITs could be sustainably used to control D. suzukii and that resistance to these techniques may only emerge in the long-term if they ever do. Field experiments will be developed in 2021 and used as quality control indicators of produced sterile males to further optimise sterile insect releases efficiency. These trials will help a large implementation of SITs, an ecologically friendly agricultural practice that can reduce the use of pesticides in France and in Europe, accordingly to the French Ecophyto II Plan and EU Directive 2009/128/EC on the sustainable use of pesticides.
Male D. suzukii or the spotted-wing drosophila. Image courtesy of J. Froissard and A. Debelle.