Drosophilidae feeding on animals and the inherent mystery of their parasitism

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Drosophilidae feeding on animals and the inherent mystery of their parasitism Jan Máca1 and Domenico Otranto2*

Abstract Insect evolution, from a free to a parasitic lifestyle, took eons under the pressure of a plethora of ecological and environmental drivers in different habitats, resulting in varying degrees of interactions with their hosts. Most Drosophilidae are known to be adapted to feeding on substrates rich in bacteria, yeasts and other microfungi. Some of them, mainly those in the Steganinae subfamily, display a singular behaviour, feeding on animal tissues or secretions. This behaviour may represent an evolving tendency towards parasitism. Indeed, while the predatory attitude is typical for the larval stages of a great proportion of flies within this subfamily, adult males of the genera Amiota, Apsiphortica and Phortica display a clearly zoophilic attitude, feeding on the lachrymal secretions of living mammals (also referred as to lachryphagy). Ultimately, some of these lachryphagous species act as vectors and intermediate hosts for the spirurid nematode Thelazia callipaeda, which parasitizes the eyes of domestic and wild carnivores and also humans. Here we review the scientific information available and provide an opinion on the roots of their evolution towards the parasitic behaviour. The distribution of T. callipaeda and its host affiliation is also discussed and future trends in the study of the ecology of Steganinae are outlined. Keywords: Drosophilidae, Steganinae, zoophagy, parasitism, lachryphagy, Phortica variegata, Thelazia callipaeda

Introduction Initial stages of parasitism in insects

Insects and arachnids of medical and veterinary concern (e.g., mosquitoes, sand flies, stable flies, black flies, and ticks) have been studied extensively over the centuries, primarily because of the effect of their parasitic feeding habits on many species of domestic and wild animals, and humans. Indeed, these arthropods affect the health, welfare and production of animals through the transmission of disease-causing pathogens or just through biting them, therefore causing blood loss, allergic reactions, and/or nuisance and disturbance [1]. Evolution of arthropods, from a free to a parasitic lifestyle, took eons under the pressure of a wide range of ecological and environmental drivers, resulting in varying degrees of interactions with their hosts, e.g. from virtually necrophagous larvae, occasionally also causing facultative myiasis, to obligate parasitism. However, scientific information on the insect taxa that evolved only partial * Correspondence: [email protected] 2 Department of Veterinary Medicine, University of Bari, 70010, Valenzano, Bari, Italy Full list of author information is available at the end of the article

parasitic interactions with their hosts, is scant [2,3], and it puts them in a group of organisms of an as yet undefined parasitic status. For example, most Drosophilidae are known to be adapted to feeding on substrates rich in bacteria, yeasts and other fungi (e