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Final Report Summary - BIOMODICS (Biological Control as a model system to investigate the factors affecting the establishment and dynamics of introduced populations)

Invasive species can severely affect biodiversity, economy and human or animal health in the regions they invade. In agricultural systems, for example, invasive pests often establish in new areas with few or no natural enemies from their native region, and their populations subsequently increase in density and can be costly to manage. In such situations, a commonly used management method, providing long-term regulation of the invasive pests, is classical biological control. It consists in the importation of natural enemies to regulate the populations of the exotic invasive pest. Classical biological control is by its very nature an international R&D activity, because invasive pests most commonly affect more than one country, and their management requires collaboration with experts from their native region. However, most research financing schemes are national and little adapted to such international activities. A first objective of BIOMODICS was to demonstrate how international staff exchange programmes can greatly benefit to international classical biocontrol initiatives.
Classical biological control is also a particularly well-suited system to study the factors (demographic, genetic, and environmental) influencing the dynamics of animal populations establishing in a new environment, which correspond to a timely research question in evolutionary biology. Targeting this question requires experimental approaches, in which factors can be manipulated and isolated. Classical biological control is a particularly appropriate model system to develop such approaches because it offers the exceptional opportunity to manipulate the characteristics of introduced natural enemy populations and their conditions of introductions, be it in the laboratory (when imported from the native region of the exotic pest) or in the field (when natural enemies are field released).
The project Biomodics joins the forces of five research institutions from France, Spain, Chile, New Zealand and South Africa, with the aim to carry out several classical biological control programmes benefitting from international collaborations, and taking profit of these programmes to address the evolutionary ecology topic described above. The classical biological control programmes considered several target pests of economic relevance both in the European Union and the partner countries: the codling moth Cydia pomonella (Lepidoptera: Tortricidae) infesting apple orchards, and the scale insects Delottococcus aberiae, Planococcus ficus (Hemiptera: Pseudococcidae) and Protopulvinaria pyriformis (Hemiptera: Coccidae) affecting citrus orchards and vineyards. The project focused on different steps in each of these programmes. The programme against the codling moth was already advanced before Biomodics, with first releases of a candidate biocontrol agent, the micro-wasp, Mastrus ridens (Hymenoptera: Ichneumonidae). The others were at earlier stages of development, with the priority need to survey natural enemies at the international scale to identify candidate biological control that could be later introduced into European Citrus orchards.
As a consequence, two main types of activities were planned in Biomodics: (i) the sampling and characterization, with molecular and morphological methods, of pests and natural enemies, be it to look for adequate biocontrol agents, or to prepare their future field releases; (ii) laboratory and field experiments, investigating the factors affecting the performance and establishment success of biocontrol agents.
Biomodics enabled to coordinate the actions of three different countries (Chile, France, New Zealand) on the management of the codling moth through the introduction of M. ridens. It allows the progress of each country until the stage of field release: field releases, coupled with experimental designs testing for the impacts of genetic diversity and landscape structure, could be carried out in Chile (2016-2017) and New Zealand (2015-2016) and Biomodics results enabled the French teams to get M. ridens material and introduction authorization within a very short period of time, making it possible to plan the first field releases in 2018 (Muru et al, 2018). Characterisation of M. ridens populations with genetic markers developed in Biomodics also led to the discovery of a genetic mechanism, the “Single-Locus Complementary Sex-Determinism” (sl-CSD), accounting for effects of genetic diversity on population performance (Retamal et al. 2016). In species with sl-CSD, the sex of individuals is determined by the CSD gene. When a diploid individual displays two different versions of the gene, it develops as a female. When both chromosomes of a diploid individual display a same version of the CSD gene, the individual develops as a male generally with lower fitness, which is detrimental to the whole population. In inbred populations, in which genetic diversity is low, the probability for individuals to carry a single version of the CSD gene is higher, which generates higher rates of unfit males and can affect establishment capacity. The impacts of sl-CSD on M. ridens populations was further investigated in laboratory experiments and confirmed, with notably a strong impact of inbreeding on Mastrus ridens as a likely consequence of the sl-CSD mechanism (Bueno et al., 2017; Zaviezo et al., 2018; Zaviezo et al., in prep.). However, interestingly, M. ridens diploid males could generate females in their progeny, which is not always the case in insects (Zaviezo et al., 2018). The detection of sl-CSD in this biocontrol programme is also a major opportunity to investigate the effects of this genetic mechanism at the population level in establishing populations. Biomodics thus promoted this biocontrol agent as a model system on which the teams will focus within the next years. The field releases carried out in 2016 and 2017 were designed to test for the effects of sl-CSD and results to be gathered in 2018-2020 are particularly promising.
In the biocontrol programmes against scale insects, the combined expertise of EU, South African and Chilean teams made it possible to progress faster on the characterization of pests and natural enemies. The collection and characterization of hundreds of field samples revealed unexpected complexity within the populations supposedly belonging to Delottococcus aberiae, Planococcus ficus, and Protopulvinaria pyriformis. These species were found to consist of several genetically differentiated populations, and candidate natural enemies could be identified for each of them (Beltrà et al., 2015; Benito et al., in prep.). Rearings of the pests could be established in the laboratory in Spain and allowed the rearing of parasitoids to prepare the future biocontrol releases. Field Experiments were also conducted to investigate factors affecting the performance of biological control. One of these experiments revealed an association between pests and ants, the latter interfering with the action of biocontrol agents (Beltrà et al. 2017). This unprecedented effort of sampling and characterization at the international level paves the way for the planned biocontrol releases and more generally for the management of several of the most important phytosanitary problems of EU orchards.
Biomodics was also configured to involve in priority early-stage researchers and provide them with a rich international R&D experience. In total, 11 early-stage researchers performed international mobilities of over three months and were integrated to the teams at the receiving institutions to develop the activities presented above.
References cited:
• Beltra, A., P. Addison, J.A. Avalos, D. Crochard, F. Garcia-Mari, E. Guerrieri, J.H. Giliomee, T. Malausa, C. Navarro-Campos, F. Palero, and A. Soto. 2015. Guiding Classical Biological Control of an Invasive Mealybug Using Integrative Taxonomy. PloS One 10.
• Beltrà A., Navarro-Campos C, Calabuig A , Estopà L, Wäckers FL , Pekas A , Soto A. 2017. Association between ants (Hymenoptera: Formicidae) and the vine mealybug (Hemiptera: Pseudococcidae) in table-grape vineyards in Eastern Spain. Pest Management Science 73: 2473-2480.
• Bueno, E., A. Romero, I. Osorio, & T. Zaviezo. 2017. Laboratory rearing methods that promote inbreeding have a negative impact in the fitness of Mastrus ridens Horstmann (Hymenoptera: Ichneumonidae), a parasitoid used for the control of codling moth. Chilean Journal of Agricultural Research 77: 413 - 419. doi:10.4067/S0718-58392017000400413
• Muru D, Alexandra Auguste, Xavier Fauvergue, Thibaut Malausa, Nicolas Ris, Marcel Thaon, Élodie Vercken Et Nicolas Borowiec. 2018. Un parasitoïde exotique pour lutter contre le carpocapse. Phytoma 710 : 37-41.
• Retamal R, Zaviezo T, Malausa T, Le Goff, I, Toleubayev K. Genetic Analyses of Field and Laboratory Populations of Mastrus ridens (Hymenoptera: Ichneumonidae), a Parasitoid of the Codling Moth, Using Microsatellite Markers. Biological Control 101: 69-77
• Zaviezo T, Retamal R, Urvois T, Fauvergue X, Blin A, Malausa T. 2018. Effects of inbreeding in a gregarious parasitoid wasp with complementary sex determination. Evolutionary Applications 11: 243-253. DOI: 10.1111/eva.12537

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