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Neighbor-Joining tree for COI and correspondence with ITS2 The labels for haplotypes concatenate information separated by hyphens as follows (from left to right): Either the GenBank accession or a haplotype number referring to internal identifiers in the Institute Sophia Antipolis (see table S2); the related amino-acid haplotype (from A to G) after translation using the invertebrate mitochondrial code; and when available, the related ITS2 haplotype (its2_a, its2_b, or its2_c) (also see table S2). The haplotypes marked with an asterisk (*) present mutations associated to a change of the biochemical nature of the corresponding amino acid.
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Uncertainty about the taxonomic status and the specificity of a species commonly prevent its consideration as a candidate for biological control of pest organisms. Here we use a combination of molecular analysis and crossing experiments to gather evidence that the parasitoid wasp Ganaspis brasiliensis, a candidate for biological control of the inva...
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Simple Summary
Soft fruit is an economically important global fruit crop. Drosophila suzukii is a significant pest of soft fruit, including grape bayberry. In China, Trichopria drosophilae is the dominant pupal parasitoid of D. suzukii. In order to control the population of D. suzukii more effectively and reduce the use of pesticides, researchers h...
Drosophila suzukii is an important fruit pest of global significance. The combined application of insecticides and natural enemies can control D. suzukii efficiently and reduce chemical insecticide residues. The pupal parasitoid Trichopria drosophilae has been evaluated for the biological control of D. suzukii . However, little is known about the t...
Based on host specificity and distribution data, it has been hypothesized that Ganaspis brasiliensis (Ihering, 1905), a natural enemy of the horticultural pest spotted-wing drosophila, Drosophila suzukii Matsumura, 1931 (SWD), was composed of multiple, cryptic species. Parasitoid wasps assigned to the species name Ganaspis brasiliensis and Ganaspis...
Citations
... kimorum) or more likely G3 (Ganaspis lupini Buffington) as supposed by the authors. Given that G. kimorum and G. lupini differ in many biological, ecological and genomic traits (Seehausen et al., 2020;Hopper et al., 2024;Stahl et al., 2024b), the outcome of larval/pupal parasitoid interactions needs to be thoroughly investigated in G. kimorum to predict potential interspecific impact on the ongoing CBC program. This becomes even more important considering that both P. vindemiae and T. drosophilae can forage in the canopy and on the ground, interacting with D. suzukii and other nontarget drosophilid puparia , which may have been previously attacked by G. kimorum or other larval parasitoids such as Leptopilina heterotoma (Thomson) (Hymenoptera: Figitidae) (Quicray et al., 2023). ...
... Modern molecular tools are easily able to characterise sibling species and biotypes and their use should be part of all CBC programmes (Hoddle et al. 2015). Sibling species, biotypes, and populations of parasitoids and predators used in CBC can differ in traits such as host specificity (Derocles et al. 2016;Seehausen et al. 2020), climatic suitability (van den Bosch et al. 1970;Valente et al. 2017), encapsulation resistance (Pschorn-Walcher and Zinnert 1971), microhabitat preference (Kenis and Mills 1998;Seehausen et al. 2020) diapause requirements (Kenis et al. 1996), and various other reproduction and development characteristics (see examples in Caltagirone 1985 andHopper et al. 1993). ...
... Modern molecular tools are easily able to characterise sibling species and biotypes and their use should be part of all CBC programmes (Hoddle et al. 2015). Sibling species, biotypes, and populations of parasitoids and predators used in CBC can differ in traits such as host specificity (Derocles et al. 2016;Seehausen et al. 2020), climatic suitability (van den Bosch et al. 1970;Valente et al. 2017), encapsulation resistance (Pschorn-Walcher and Zinnert 1971), microhabitat preference (Kenis and Mills 1998;Seehausen et al. 2020) diapause requirements (Kenis et al. 1996), and various other reproduction and development characteristics (see examples in Caltagirone 1985 andHopper et al. 1993). ...
More than a century ago, a few successful pest control attempts through the intentional import and release of insects, opened the way for the practice of biological control. Since then, the shipment of beneficial insects within and between continents became common practice and was solely based on informal arrangements between researchers and practitioners. However, over the last three decades, worldwide there has been an increased awareness of both perceived and real environmental risks potentially posed by biological control agents. Consequently, countries around the world started implementing legislations and regulations regarding biological control, although most of the time only indirectly via other legislations, such as those concerning plant health, pesticides or the environment. Here we describe the development and key events that influenced the transition from the early days of biological control without regulations, to the implementation of national policies and the more recent attempts for regional and worldwide harmonization of regulations. Because most legislations and regulations regarding biological control concern all environments, we present here a very general overview and include examples from forestry where appropriate. Through the course of historical events and changing views on environmental issues, value of natural resources and pest control, biological control faced many challenges. While researchers and practitioners currently have to navigate through a jungle of policies, biological control is now in the spotlight again as an environmentally sound tool to tackle plant pests and diseases. Certain policies continue to impede biological control in some countries, but some can also be regarded as crucial instruments to improve this pest control method and consequently its application as a powerful and safe practice.
... A better description of host use by G. kimorum and G. lupini may be deduced from recent quarantine studies in Switzerland (Girod et al. 2018a, Seehausen et al. 2020) and California (Giorgini Daane et al. 2021). Natural enemy selection for classical biological control programs now emphasizes increased host specificity to reduce risk to non-target species Cock 2018, Hoddle et al. 2021). ...
... With a better understanding of host preference within the Ganaspis spp. complex, Seehausen et al. (2020) showed that G. lupini readily attacked D. suzukii, D. melanogaster, and D. simulans whereas G. kimorum showed a strong preference for D. suzukii in fresh undamaged fruit but could, under laboratory conditions, attack D. melanogaster as well. ...
... Other field evidence includes reports that G. kimorum populations in Japan only attacked D. suzukii-infested cherries (Prunus spp.) in ripening fruit (Nomano et al. 2017, Girod et al. 2018b, Matsuura et al. 2018. In contrast, G. kimorum populations from South Korea and (Kunming) China may prefer D. suzukii but have a slightly broader host range than the (Tokyo) Japanese material studied by Girod et al. (2018b) and Seehausen et al. (2020). To better understand the ecological host range, Seehausen et al. (2022) conducted a largearena field cage study with G. kimorum (Tokyo) exposed to D. suzukii larvae in fresh fruits (blueberries Vaccinium sp. ...
Ganaspis Foerster includes several cryptic species that are important larval parasitoids of the invasive pest Drosophila suzukii (Matsumura), spotted-wing drosophila (SWD). Drosophila suzukii, native to Asia, was first discovered in 2008 in North America and Europe, becoming a devastating pest of soft-skinned fruit crops. Biological control could be among the safest, most environmentally benign, and cost-effective methods for long-term and landscape-level management of this invasive pest. Foreign exploration in East Asia discovered several major larval
D. suzukii parasitoids. One of them was initially described as Ganaspis brasiliensis (Ihering) and consisted of 2 major genetic groups (G1 and G3). The groups are now recognized as 2 different species, Ganaspis kimorum Buffington and Ganaspis lupini Buffington. The more host-specific species G. kimorum was selected and approved for field release in the United States in 2021 and has been widely released since 2022. Here, we provide a comprehensive overview of the parasitoid’s taxonomy, current known distribution, biology, ecology, mass-rearing methods, and
biological control potential.
... Recently, taxonomists shed light on the taxonomic status of this complex of cryptic species and redescribed the released G1 lineage as Ganaspis kimorum Buffington and the G3 as G. lupini Buffington (Sosa-Calvo et al. 2024). Ganaspis kimorum and G. lupini are reproductively incompatible and display considerable differences in whole-genome sequences (Seehausen et al. 2020, Hopper et al. 2024. A more recent USDA APHIS petition approved the release of G. kimorum throughout the continental United States. ...
... Reproduction of coldstored male wasps is a parameter that should be considered by future research as it can affect the population dynamic of the parasitoid. As an example, G. kimorum is an arrhenotokous species and unmated females give birth only to male offspring (Seehausen et al. 2020). Future post-storage quality assessment should also focus on other parameters that have been rarely considered in such evaluations, such as the dispersal ability, foraging and mating behaviors, intergenerational effects, and procedures to evaluate and/or improve shipment and handling of the natural enemy to avoid deterioration of the biocontrol agents (van Lenteren andTommasini, 1999, Colinet andBoivin, 2011). ...
Programs to mass rear and release Ganaspis kimorum Buffington (Hymenoptera: Figitidae) are ongoing in many countries to manage its host Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). To optimize parasitoid production and synchronize field releases with pest outbreaks, we investigated a cold storage protocol by exposing different immature G. kimorum stages to 2 storage temperatures (10 or 15°C) for 2, 4, 6, or 8 wk. We further studied those temperature/exposure time combinations that allowed survival but prevented parasitoid emergence before the end of each cold exposure, or the cold storage suitability (CSS). The impact of cold storage on G. kimorum emergence time, total development time, and emergence rate was then evaluated for temperature/exposure time combinations with CSS > 60%. We also assessed fitness costs in terms of longevity and parasitism rates of emerging parasitoids. Results showed that only G. kimorum larvae and pupae were suitable for cold storage under this methodology. Cold exposure significantly delayed the emergence time and total development time of larvae and pupae, whereas the emergence rate was significantly reduced only for larvae at 10°C for 6 wk. The longevity of emerging male and female parasitoids was significantly reduced when stored cold as larvae, while no effects were reported for the parasitism rate by emerged females. These findings provide new insights into G. kimorum cold sensitivity and offer valuable options to better schedule mass rearing and wasp releases for biological control of D. suzukii.
... In this context, understanding the reproductive status among populations of biological control agents can be crucial to predict the success of multiple introductions and subsequent admixture impact on pest control efforts (Stouthamer et al. 2000;Dayrat 2005;Gebiola et al. 2016). To this aim, laboratory cross-breeding experiments and analyses of genetic diversity of different geographical populations through DNA barcode sequencing or genome assembly can play an essential role in the taxonomic identification and detection of cryptic species, especially for parasitoids employed as biological control agents (Desneux et al. 2009;Seehausen et al. 2020). Here, we investigate two populations of Ganaspis kimorum Buffington, 2024 (Hymenoptera, Figitidae), one of the main parasitoids attacking the spotted-wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera, Drosophilidae). ...
... When it was first reported from Japanese field collections of wild cherries infested by D. suzukii, it was assigned as the suzukii-type of G. xanthopoda Ashmead (Kasuya et al. 2013) and then later as G. brasiliensis (e.g., Buffington and Forshage 2016;Daane et al. 2016;Giorgini et al. 2019) or G. cf. brasiliensis (e.g., Girod et al. 2018a;Seehausen et al. 2020). Nomano et al. (2017) divided the G. cf. ...
Taxonomic and host associations have been closely studied within the Ganaspis brasiliensis (Ihering, 1905) (Hymenoptera, Figitidae) complex as parasitoids of the spotted-wing drosophila, Drosophila suzukii (Matsumura, 1931) (Diptera, Drosophilidae). Initially, five genetic groups (G1–G5) were identified that suggested the existence of cryptic species that vary in their host ranges and geographic distributions. What was referred to as the “G1” strain was recently described as G. kimorum Buffington, 2024, and approved for release as a classical biological control agent in the United States and parts of Europe. Concurrently, an adventive population of G. kimorum was found in British Columbia, Canada and is likely spreading through parts of the Pacific Northwest such as Washington State, USA. Here, we compare the reproductive compatibility and molecular similarity of laboratory-bred G. kimorum (collected in Tokyo, Japan) used for release in the USA and Europe with the adventive population found in Washington State, USA. Cross-breeding experiments between the Tokyo and the adventive population showed successful mating and the production of female offspring, indicating that they are reproductively compatible. For both populations, the mitochondrial COI barcode region was sequenced and further confirmed the conspecificity of the Tokyo and adventive Washington populations with published G. kimorum. These findings will help to better understand and document the effects of releases of G. kimorum and the reproductive success of adventive and released populations.
... Two additional Drosophilidae species were unsuccessfully attacked (i.e., parasitoid offspring did not develop) by both G. lupini and G. kimorum (Girod et al., 2018). During the initial host range testing phase, the different lineages of Ganaspis were identified based on associations between mitochondrial 'barcode' gene (cytochrome oxidase subunit I) haplotypes and relative host specificity, and it subsequently became clear that these represent cryptic species (Kasuya et al., 2013;Nomano et al., 2017;Rossi Stacconi et al., 2019;Seehausen et al., 2020;Hopper et al., 2024). The most host-specific Ganaspis lineage, previously known as 'G1 G. brasiliensis', was recently described as a distinct species, G. kimorum (Sosa-Calvo et al., 2024). ...
Drosophila suzukii, spotted-wing drosophila, is an invasive pest in Canada that can lay its eggs into fresh fruits,
unlike many of its close relatives. Larval feeding inside fruit causes the fruit to spoil prematurely. Some parasitoids
have been found attacking D. suzukii larvae and pupae in regions that D. suzukii has invaded, including Asobara cf.
rufescens in Canada. A parasitoid from Asia, Ganaspis kimorum, has the narrowest host range of the parasitoids
identified in the native range of D. suzukii and has been approved for release in some countries. In 2019, an adventive population of G. kimorum and of another parasitoid, Leptopilina japonica, was detected in British Columbia, where research is now being conducted to determine if these parasitoids attack native species of Drosophila. The chapter also reviews the predators, pathogens, and use of sterile insect technique for biological control of
D. suzukii.
... Quarantine studies showed the koinobiont endoparasitoid G. kimorum, formerly recognized as G. cf. brasiliensis (Ihering), as the most promising natural enemy for the classical biological control of D. suzukii because of its host-specificity [40,41]. Consequently, field releases of this parasitoid are currently ongoing in Europe and the US in the framework of a classical biological control program [42,43]. ...
... A complementary bioassay consisted of insecticide-and distilled water-treated fruits, without exposure to parasitoids to evaluate the mortality of D. suzukii larvae induced by each tested insecticide. Blueberries of both bioassays (i.e., in the presence and absence of parasitism) were incubated for 30 ± 2 days at 23 ± 1 °C, 60 ± 10% R.H, and 16h:8h L:D photoperiod, and the number of emerged flies and/or parasitoids was counted to assess the G. kimorum apparent parasitism (AP), according to Seehausen et al. [40]. The AP was calculated as the proportion of emerged adult parasitoids among the total number of adult insects that emerged from blueberries [40]. ...
... Blueberries of both bioassays (i.e., in the presence and absence of parasitism) were incubated for 30 ± 2 days at 23 ± 1 °C, 60 ± 10% R.H, and 16h:8h L:D photoperiod, and the number of emerged flies and/or parasitoids was counted to assess the G. kimorum apparent parasitism (AP), according to Seehausen et al. [40]. The AP was calculated as the proportion of emerged adult parasitoids among the total number of adult insects that emerged from blueberries [40]. Both the individual and combined effects of insecticide and/or parasitoid on pest mortality were assessed. ...
Drosophila suzukii and Tuta absoluta are successful biological invaders of agroecosystems. Their integrated pest management (IPM) programs involve the release and/or conservation of natural enemies. Among these, Ganaspis kimorum is a major Asian parasitoid of D. suzukii and has been introduced as a classical biological control agent of this pest in Europe and North America, while Necremnus tutae is a key fortuitous parasitoid of T. absoluta in the Mediterranean region. Bioinsecti-cides represent key alternatives to chemicals for controlling both pests. This study investigated the potential compatibility of both parasitoids with Beauveria bassiana, Bacillus thuringiensis, garlic essential oil (EO), and spinosad, in comparison to two synthetic insecticides, cyantraniliprole and chlorantraniliprole. The results showed that combining each of the tested insecticides with G. kimorum slightly increased pest mortality compared to the insecticide alone. Necremnus tutae had a significant additive effect on host mortality when combined with insecticides. Beauveria bassiana and B. thuringiensis were most compatible with both parasitoid species. Both garlic EO and chlorantraniliprole impaired the survival of immature N. tutae and showed sublethal toxicity on the reproductive and non-reproductive behaviors of N. tutae. Spinosad exhibited high acute toxicity on both juvenile and adult parasitoids of both species. Overall, these findings provide useful insights into insecticide selectivity toward two key parasitoids and offer new knowledge on the potential of combining natural enemies and bioinsecticides for optimized IPM.
... The thorough characterization of G. brasiliensis required for its introduction revealed a high genetic variability of the species, differentiated into five main lineages, each characterized by specific bioecological features and host ranges. Therefore, the existence of a complex of cryptic species was hypothesized (Nomano et al., 2017;Giorgini et al., 2019;Seehausen et al., 2020). Among the G. brasiliensis lineages, the G1 was found to have the highest degree of host specificity. ...
... Laboratory observations confirmed all these features rendering G. brasiliensis G1 a suitable species for introduction within the framework of classical biological control programs. In fact, it was shown that G1 females rarely parasitize D. suzukii or other drosophilid larvae within artificial diets or rotting fruits (Seehausen et al., 2020). Furthermore, although the parasitoid could develop in other Drosophila species closely related to D. suzukii (i. ...
... Furthermore, although the parasitoid could develop in other Drosophila species closely related to D. suzukii (i. e., D. melanogaster Meigen and D. simulans Sturtevant) when forced to attack them in fresh fruits, it always preferred D. suzukii when given the choice (Seehausen et al., 2020). This result was even more evident in choice tests under semi-field conditions where G1 females were found to parasitize D. suzukii larvae in fresh fruits and almost no D. melanogaster larvae in rotting fruits (Seehausen et al., 2022). ...
... Ganaspis brasiliensis was, early on, recognized as a common natural enemy of SWD, and was redescribed (Buffington and Forshage 2016). Since then, additional field and lab studies (summarized by Seehausen et al. 2020) have suggested G. brasiliensis could in fact be a cryptic species complex, composed of as many as five species (Nomano et al. 2017). The study by Nomano et al (2017) reported five lineages of G. brasiliensis, namely G1-G5. ...
... Since that study, G1 has been recognized as the most host-specific population of G. brasiliensis (Giorgini et al. 2018;Abram et al. 2022) and has even been cleared for release in the United States by USDA-APHIS; G3, also a natural enemy of SWD, has a slightly broader host range, and where it co-occurs with G1, a slightly less effective natural enemy of SWD; and G5 appears to be pan-tropical and not able to exploit SWD at all; other Drosophila species are hosts for G2 and G4 (Nomano et al. 2017). Altogether, these data led Seehausen et al. (2020) to set the stage for these populations of G. brasiliensis G1, G3, and G5, to be recognized as distinct species (G2 and G4 lacked sufficient sample data). Hopper et al. (2024) presented whole genome datasets that suggest G1 and G3 are in fact separate species (although G5 was not included, as it has not been recorded attacking SWD). ...
... Further, members of G. kimorum were discovered to have a reduced ovipositor clip (Fig. 4). Research on the genome (Hopper et al. 2024), host specificity (Girod et al. 2018b;Wang et al. 2018;Seehausen et al. 2020;Daane et al. 2021), reproductive isolation (Seehausen et al. 2020;Hopper et al. 2024), and DNA barcode region (Nomano et al. 2017) are consistent with the morphological characters and UCE phylogenomic data shown here (Fig. 6). Together these data support the description of G. kimorum and G. lupini as species new to science. ...
Based on host specificity and distribution data, it has been hypothesized that Ganaspis brasiliensis (Ihering, 1905), a natural enemy of the horticultural pest spotted-wing drosophila, Drosophila suzukii Matsumura, 1931 (SWD), was composed of multiple, cryptic species. Parasitoid wasps assigned to the species name Ganaspis brasiliensis and Ganaspis cf. brasiliensis were investigated using a molecular dataset of ultra-conserved elements (UCEs) and morphology. We report strong evidence for the presence of cryptic species based on the combination of UCE data (1,379 UCE loci), host specificity, ovipositor morphology, and distribution data. We describe these new cryptic species as: Ganaspis lupinisp. nov., and Ganaspis kimorumsp. nov.Ganaspis lupini was formerly recognized as Ganaspis brasiliensis G3, and Ganaspis kimorum as Ganaspis brasiliensis G1. These two new species appear to be restricted to the temperate climates, whereas Ganaspis brasiliensis (formerly recognized as Ganaspis brasiliensis G5) has a more pan-tropical distribution. We investigated the characterization of the ovipositor clip of these species, and hypothesize that G. kimorum, which has a reduced ovipositor clip, has an advantage in ovipositing into fresh fruit, still on the host plant, while attacking SWD; as a corollary, G. brasiliensis and G. lupini, which both have a larger ovipositor clip, are better adapted to attacking hosts in softer, rotting fruit on the ground. As Ganaspis kimorum was authorized for release as a biological control agent against SWD under the name Ganaspis brasiliensis G1, the results here have direct impact on the field of biological control.
... Indeed, four to five genetic groups (G1-G5), mainly differing in the host range, were identified in the G. cf. brasiliensis complex (Nomano et al. 2017;Giorgini et al. 2019;Seehausen et al. 2020). Among these, the G1 strain resulted as the most hostspecific lineage mostly parasitizing D. suzukii larvae within fresh and ripe fruits (Girod et al. 2018a;Seehausen et al. 2022). ...
Background
The spotted wing drosophila, Drosophila suzukii, is an invasive pest causing significant economic losses worldwide. Current pest control strategies mainly rely on insecticides, which negatively impact fruit marketability and the sustainability of integrated pest management (IPM) programs. In addition, pesticides can have dramatic consequences on non-target species when persisting in the environment at low concentrations after field applications. In this context, chemical control can strongly interfere with the releases of the G1 strain of the Asian larval parasitoid Ganaspis cf. brasiliensis, which is currently the adopted classical biological control agent to manage D. suzukii infestations worldwide.
Methods
Probit analysis was used to assess the baseline toxicity of acetamiprid, cyazypyr, lambda-cyhalothrin, phosmet, and spinosad on G1 G. cf. brasiliensis adults through residual contact exposure in the laboratory. Then, adult parasitoids were exposed to insecticide low Lethal Concentrations (LC5 and LC30) and their mortality was checked daily to assess the survival of treated wasps.
Results
Lambda-cyhalothrin showed the highest toxicity on the parasitoid with a LC50 of 1.38 × 10–3 g active ingredient (a.i.) /L, while cyazypyr seemed the safer active ingredient with an estimated LC50 of 0.20 g a.i./L without affecting parasitoids at sublethal doses. Spinosad and phosmet significantly reduced wasp survival at both LC30 and LC5, while lambda-cyhalothrin and acetamiprid affected parasitoid lifespan only at LC30. Spinosad, lambda-cyhalothrin and phosmet LC30 caused the major survival reductions, followed by acetamiprid LC30. The least significant reduction in parasitoid survival was 21.6% by spinosad LC5.
Conclusions
Overall, this study highlighted the importance of carefully selecting insecticides to minimize adverse effects on non-target organisms. In particular, cyazypyr was the most promising candidate to integrate inoculative biological control with chemical treatments. By contrast, the application of phosmet, spinosad and lambda-cyhalothrin should be avoided alongside parasitoid field releases. Although acetamiprid is less used against D. suzukii in the field than the other tested molecules, it should be used with caution due to its sublethal toxicity on the parasitoid. These results provide the first evidence of G. cf. brasiliensis susceptibility to insecticides in order to promote sustainable and efficient pest management strategies.
