Olfactory responses of the variegated fruit fly, Phortica variegata, an emerging vector of the zoonotic eyeworm Thelazia callipaeda, to ecologically relevant volatiles.

Abstract

Background: The variegated fruit fly, Phortica variegata (Drosophilidae: Steganinae), is native to Europe and has emerged as a major vector of ocular nematosis caused by Thelazia callipaeda (Rhabditida: Thelaziidae), following the its introduction into Europe from Asia. Male P. variegata transmit these nematodes by feeding on tears of mammals, including wild and domestic carnivores (foxes, beech martens, wild cats, and dogs), lagomorphs, and humans. Understanding the olfactory responses of P. variegata to volatile cues is essential for developing attractant-based surveillance and control strategies, yet its olfactory ecology remains largely unexplored.

Methods: We used gas chromatography coupled electroantennography to measure antennal responses to synthetic and natural volatile blends. A comparative analysis was performed on the antennal responses of both sexes of P. variegata and its well-studied relative, Drosophila melanogaster. Components of the synthetic blends were selected based on the odorant receptor repertoire of D. melanogaster and established mosquito attractants, with the rationale that conserved olfactory receptors among dipterans may allow P. variegata to detect similar compounds. Volatile extracts collected using active carbon adsorbent traps were also tested on the antennae and analyzed using gas chromatography coupled mass spectrometry.

Results: Male P. variegata showed higher antennal responses to phenol, 3-octanone, and sulcatone than females, indicating olfactory sexual dimorphism. Compared to D. melanogaster, the antennae of P. variegata did not respond to several common plant alcohols and terpenoids. Instead, they showed stronger responses to compounds such as anisole, ethyl propanoate, butyl propanoate, propyl acetate, 3-octanone, nonanal, and decanal, suggesting that peripheral olfaction in P. variegata may be more tuned to microbial volatiles.

Conclusions: Phortica variegata exhibits sexual dimorphism in olfactory responsivity, with males showing greater responsiveness to volatiles associated with host-seeking in other zoophilic dipterans, potentially guiding them to mammalian hosts for tear-feeding. Compared to D. melanogaster, P. variegata is more responsive to microbial and yeast-related volatiles and less responsive to plant-derived terpenoids, suggesting a foraging ecology linked to microbial substrates. The antennally detected volatiles identified in this study can be used as candidates for further behavioral studies to develop lures for vector management.