The Drosophila-parasitizing wasp Leptopilina heterotoma: A comprehensive model system in ecology and evolution

Abstract

The parasitoid Leptopilina heterotoma has been used as a model system for more than 70 years, contributing greatly to diverse research areas in ecology and evolution. Here, we synthesized the large body of work on L. heterotoma with the aim to identify new research avenues that could be of interest also for researchers studying other parasitoids and insects. We start our review with a description of typical L. heterotoma characteristics, as well as that of the higher taxonomic groups to which this species belongs. We then continue discussing host suitability and immunity, foraging behaviors, as well as fat accumulation and life histories. We subsequently shift our focus towards parasitoid-parasitoid interactions, including L. heterotoma coexistence within the larger guild of Drosophila parasitoids, chemical communication, as well as mating and population structuring. We conclude our review by highlighting the assets of L. heterotoma as a model system, including its intermediate life history syndromes, the ease of observing and collecting natural hosts and wasps, as well as recent genomic advances.

Keywords: associative learning; endosymbiont; fitness; host‐parasitoid community; lipids; sex pheromones; virulence.

FIGURE 1

The amber wasp Leptopilina heterotoma © Hans Smidt

FIGURE 2

Lateral view of the thorax of Leptopilina heterotoma (a) and Asobara tabida (b) with the scutellum highlighted with a red line. Dorsal view of the scutellum for L. heterotoma (c) and A. tabida (d). The scutellar plate common to eucolines is highlighted with the green line, and the glandular pit with the blue dot.

FIGURE 3

Development of Leptopilina heterotoma. Timeline of the developmental stages of Drosophila melanogaster (green), and L. heterotoma developing in D. melanogaster (blue) at 25°C. Numbers indicate the time in days (adapted from van Alphen & Thunnissen, 1983). L. heterotoma goes through three larval stages (Carton et al., ; Jenni, 1951) that may differ depending on the temperature and the host species used (Howe, ; Jenni, 1951). A female can oviposit in all larval host instars, but survival is highest when eggs are laid in second instar (Jenni, 1951). After ~30–34 h, the embryo possesses 10 segments (corresponding to the three thoracic and seven abdominal segments of the adult) that are clearly visible (Jenni, 1951). The egg then hatches after ~39–49 h, with females hatching approximately 3 h later than males (Eijsackers & Bakker, 1971). The first larval instar possesses caudal and thoracic appendages, and the larva uses its mandibles mainly to consume host hemolymph (Carton et al., ; Jenni, 1951). The first molt of the parasitoid takes place at approximately the same time as host pupation (Carton et al., 1986), which may have a similar hormonal basis (Kopelman & Chabora, 1984). From the second instar onwards, larvae use their mandibles to feed on the host's tissues (Carton et al., 1986). At the time of the second molt, the parasitoid leaves the host's body and lies in between the pupa and the puparium feeding as an ectoparasitoid (Carton et al., 1986). The third larval instar has a much rounder shape than the earlier instars and does not bear any appendages anymore. In the pre‐pupal stage, the larva loses its mandibles (Jenni, 1951) and excretes pellets (meconia) that become visible at the posterior end of the host puparium (Carton et al., ; Jenni, 1951). Pupation lasts approximately 9 days (Jenni, 1951) and the parasitoid becomes gradually pigmented (Jenni, ; van Alphen & Thunnissen, 1983). The time of emergence is ~21 days after oviposition for males, and ~23 days for females. After emerging from its own puparium, the adult L. heterotoma remains within the host's puparium for ~24 h before emergence (van Alphen & Thunnissen, 1983).

FIGURE 4

Lifestyle characteristics of the four main wasp families parasitizing Drosophila. Each family is visually represented by a common species: Figitidae—Leptopilina heterotoma, Braconidae—Asobara tabida, Pteromalidae—Pachycrepoideus vindemmiae, Diapriidae—Trichopria drosophilae. Eggs of ectoparasitoids are laid on the outside of the host, whereas those of endoparasitoids are laid inside the host. Endoparasitoid larvae may, however, develop some time outside the host body, depending on the species (see Figure 3 for L. heterotoma where this occurs; Harvey & Strand, 2002).

FIGURE 5

Phylogeny of the genus Leptopilina, redrawn from Novkovic et al. (2011) and Buffington et al. (2020).

FIGURE 6

The two types of cytoplasmic incompatibility induced by Wolbachia in haplodiploid insects: the Male Development type described in Nasonia vitripennis (Breeuwer & Werren, 1990) and the Female Mortality type described in Leptopilina heterotoma (Vavre et al., 2000, 2001). f: Wolbachia‐free, w: infected with Wolbachia (wNvitA and wNvitB for N. vitripennis; wLhet1, wLhet2 and wLhet3 for L. heterotoma).