The Olfactory System of Dolichogenidea gelechiidivoris (Marsh) (Hymenoptera: Braconidae), a Natural Enemy of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)

Abstract

The parasitoid wasp Dolichogenidea gelechiidivoris is a key koinobiont solitary endoparasitoid of the invasive agricultural pest Tuta absoluta. This study investigates both the morphological and molecular foundations of sex-specific olfactory differentiation in this species. Morphological analysis revealed that males possess significantly longer antennae (2880.8 ± 20.36 μm) than females (2137.23 ± 43.47 μm), demonstrating pronounced sexual dimorphism. Scanning electron microscopy identified similar sensilla types on both sexes, but differences existed in the length and diameter of specific sensilla. Transcriptomic analysis of adult antennae uncovered molecular differentiation, identifying 11 odorant-binding proteins (OBPs) and 20 odorant receptors (ORs), with 27 chemosensory genes upregulated in females and 4 enriched in males. Integrating morphological and molecular evidence demonstrates complementary sexual specialization in the olfactory apparatus of D. gelechiidivoris. Linking these findings to the potential functions of different sensilla types, as discussed in the context of prior research, provides crucial insights into the sex-specific use of volatile cues. These findings provide critical insights into the use of volatile signals in this highly relevant species for biological control targeting T. absoluta.

Keywords: Braconidae; Dolichogenidea gelechiidivoris; antennal sensillum; microstructures; odorant receptors (ORs); odorant-binding proteins (OBPs).

Figure 1

D. gelechiidivoris adults and parasitism behavior on T. absoluta larvae. (A) Female parasitic wasp searching for an oviposition site on a T. absoluta larva. (B) Female wasp parasitizing a T. absoluta larva. (C) Morphology of a male adult. (D) Morphology of a female adult.

Figure 2

Morphological characteristics of the antennae of female and male adults of D. gelechiidivoris and comparative measures. (A) Antenna of female and male showing the radicle (Ra), scape (Sc), pedicel (Pe), flagellum (F). Scanning electron micrograph of (B) scape and pedicel, (C) flagellum subsegment, and (D) tip of antenna excised from a D. gelechiidivoris antenna. (E) Lengths of sampled female and male (Sc–F16) antennomeres. Different lowercase letters above bars indicate significant differences between males and females (independent sample t-test, p < 0.05).

Figure 3

Schematic diagram of antennal sensilla morphology and distribution in male and female D. gelechiidivoris.

Figure 4

Morphological characteristics of some antennal sensilla of D. gelechiidivoris female and male adults. (A) Böhm’s bristles (BB), (B) sensilla trichodea I (STI) and sensilla trichodea II (STII), (C) sensilla placodea I (SPI), sensilla placodea II (SPII), sensilla basiconica I (SBI), and sensilla basiconica II (SBII), (D) sensilla placodea I (SPI) and sensilla placodea II (SPII), (E) sensilla basiconica I (SBI), and (F) sensilla basiconica II (SBII).

Figure 5

Morphological characteristics of some antennal sensilla of D. gelechiidivoris female and male adults: (A) sensilla chaetica (SCh), (B) sensilla squamous (SS) and sensilla campaniformia (SCa), (C–E) sensilla coeloconica (SCo), and (F) smell pores (SPo).

Figure 6

Heatmap of odorant-binding protein gene (OBP) and olfactory receptor gene (OR) expression levels between female and male antennae. The data were visualized using a color-coded scale ranging from blue (low expression) to red (high expression), with values normalized between −1.5 and 1.5. Hierarchical clustering was performed to group samples and genes based on expression patterns, as indicated by the dendrograms at the top and left side of the heatmap.