Limited gains in native parasitoid performance on an invasive host beyond three generations of selection

Abstract

Co‐evolved natural enemies provide sustainable and long‐term control of numerous invasive insect pests, but the introduction of such enemies has declined sharply due to increasing regulations. In the absence of co‐evolved natural enemies, native species may attack exotic invasive pests; however, they usually lack adaptations to control novel hosts effectively. We investigated the potential of two native pupal parasitoids, Pachycrepoideus vindemmiae and Trichopria drosophilae, to increase their developmental success on the invasive Drosophila suzukii. Replicated populations of the two parasitoids were subjected to 10 generations of laboratory selection on D. suzukii with Drosophila melanogaster serving as the co‐evolved host. We assessed developmental success of selected and control lines in generations 0, 3, and 10. Changes in host preference, sex ratio, development time, and body size were measured to evaluate correlated responses with adaptation. Both parasitoid species responded rapidly to selection by significantly increasing their developmental success on the novel host within three generations, which remained constant for seven additional generations without further improvement. The generalist parasitoid species P. vindemmiae was able to reach similar developmental success as the control populations, while the performance of the more specialized parasitoid T. drosophilae remained lower on the novel than on the co‐evolved host. There was no increase in preference towards the novel host over 10 generations of selection nor were there changes in development time or body size associated with adaptation in either parasitoid species. The sex ratio became less female‐biased for both parasitoids after three generations of selection but rebounded in P. vindemmiae by generation 10. These results suggest that a few generations of selection may be sufficient to improve the performance of native parasitoids on invasive hosts, but with limits to the degree of improvement for managing invasive pests when exotic co‐evolved natural enemies are not available.

Biological control potential of a laboratory selected generalist parasitoid versus a co‐evolved specialist parasitoid against the invasive Drosophila suzukii

“…Since the testing and approval of natural enemies for these so-called classical biological control introductions can take a long time, often decades, and because there has been a steep decline in such programs (Heimpel & Cock, 2018;Van Driesche et al, 2020), alternative approaches are being explored. One such alternative is to use natural enemies that are already present in the introduced ranges (Jarrett et al, 2022;Kruitwagen et al, 2018;Linder et al, 2022).…”

“…However, when an exotic host invades a novel habitat, generalist parasitoids are usually the first to attack them (Abram et al, 2019;Chris Gröbler & Lewis, 2008;Cornell & Hawkins, 1993;Grabenweger et al, 2010;Lee et al, 2019), and it is usually generalist parasitoids that respond rapidly to selection on novel hosts (Golec et al, 2019;Henry et al, 2008;Jarrett et al, 2022;Jones et al, 2015;Linder et al, 2022).…”

“…In the introduced range of the United States, only two generalist pupal parasitoids, Pachycrepoideus vindemmiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria drosophilae (Perkins) (Hymenoptera: Diapriidae), are known to attack D. suzukii at low levels (<10% parasitism rates) (Lee et al, 2019). Previous studies showed that laboratory selection could significantly increase the developmental success of these two parasitoid species on D. suzukii (Jarrett et al, 2022;Linder et al, 2022). Recently, a classical biological control agent, the specialist larval parasitoid, Ganaspis brasiliensis (Ihering) (Hymenoptera: Figitidae) was approved for field releases in North America against D. suzukii (Daane et al, 2021).…”

“…Since the testing and approval of natural enemies for these so‐called classical biological control introductions can take a long time, often decades, and because there has been a steep decline in such programs (Heimpel & Cock, 2018; Van Driesche et al, 2020), alternative approaches are being explored. One such alternative is to use natural enemies that are already present in the introduced ranges (Jarrett et al, 2022; Kruitwagen et al, 2018; Linder et al, 2022). Even though native species often lack adaptations to effectively attack exotic species, an increasing number of studies demonstrate that a few generations of laboratory selection can significantly improve the developmental success of natural enemies on novel hosts (Henry et al, 2008; Hopper et al, 2021; Jarrett et al, 2022; Jones et al, 2015; Linder et al, 2022).…”

“…These traits can make specialist parasitoids very efficient biocontrol agents with relatively high attack rates of the target species (Godfray, 1994; Hajek & Eilenberg, 2018; Heimpel & Mills, 2017; Van Driesche et al, 2020). However, when an exotic host invades a novel habitat, generalist parasitoids are usually the first to attack them (Abram et al, 2019; Chris Gröbler & Lewis, 2008; Cornell & Hawkins, 1993; Grabenweger et al, 2010; Lee et al, 2019), and it is usually generalist parasitoids that respond rapidly to selection on novel hosts (Golec et al, 2019; Henry et al, 2008; Jarrett et al, 2022; Jones et al, 2015; Linder et al, 2022). Even though generalists, by definition, are adapted to attack a wide range of species, their parasitism rates can vary widely both on native and exotic hosts (Chris Gröbler & Lewis, 2008; Cornell & Hawkins, 1993; Grabenweger et al, 2010).…”