The characterization of the circadian clock in the olive fly Bactrocera oleae (Diptera: Tephritidae) reveals a Drosophila-like organization

Abstract

The olive fruit fly, Bactrocera oleae, is the single most important pest for the majority of olive plantations. Oxitec’s self-limiting olive fly technology (OX3097D-Bol) offers an alternative management approach to this insect pest. Because of previously reported asynchrony in the mating time of wild and laboratory strains, we have characterized the olive fly circadian clock applying molecular, evolutionary, anatomical and behavioural approaches. Here we demonstrate that the olive fly clock relies on a Drosophila melanogaster-like organization and that OX3097D-Bol carries a functional clock similar to wild-type strains, confirming its suitability for operational use.

Light input pathways to the circadian clock of insects with an emphasis on the fruit fly Drosophila melanogaster

“…The best-characterized circadian clock is that of the fruit fly Drosophila melanogaster (reviewed by Helfrich-Förster 2017; Top and Young 2018), but other higher fly species appear to have a comparable clock organization with some differences existing within the Drosophiliids (Codd et al 2007;Muguruma et al 2010;Menegazzi et al 2017;Beauchamp et al 2018;Bertolini et al 2018;Helfrich-Förster et al 2018). Furthermore, all higher flies appear to possess only the light-sensitive form of CRY that may contribute to entrainment Fuchikawa et al 2010;Bertolini et al 2018) and is generally regarded as the main circadian photopigment of D. melanogaster (Stanewsky et al 1998;Emery et al 2000). In addition, some fly species possess extraretinal eyelets that are metamorphized larval eyes, and like the stemmata of beetles, they are located in a posterior position of the optic lobes (Hofbauer and Buchner 1989;Malpel et al 2002;Helfrich-Förster et al 2002;Sprecher and Desplan 2008).…”

Flies as models for circadian clock adaptation to environmental challenges

“…Species of the following families have been investigated with respect to their rhythms: Tephritidae (An et al., ; An, Tebo, Song, Frommer, & Raphael, ; Bertolini et al., ; Chahad‐Ehlers et al., ; Fuchikawa et al., ; Matsumoto et al., ; Mazzotta et al., ; Miyatake et al., ), Phoridae (Bostock, Green, Kyriacou, & Vanin, ), Calliphoridae (Muguruma, Goto, Numata, & Shiga, ; Saunders, ; Smith, ; Shiga & Numata, ; Warman, Newcomb, Lewis, & Evans, ; Yasuyama, Hase, & Shiga, ), Sarcophagidae (Goto & Denlinger, ; Koštál, Závodská, & Denlinger, ; Yamamoto, Nishimura, & Shiga, ; Yamamoto, Shiga, & Goto, ), Muscidae (Codd et al., ; Bazalova & Dolezel, ; Pyza & Meinertzhagen, ; Pyza, Siuta, & Tanimura, ), and Drosophilidae (see below) (Figure a). Among these, the genetic and neuronal basis of the circadian clock was revealed for the house fly M. domestica (Codd et al., ), the blow fly Protophormia terraenovae (Muguruma et al., ) and recently also for the olive fly, Bactrocera oleae (Bertolini et al., ). In all three fly species, it turned out to be rather similar to that of the fruit fly D. melanogaster , although the families of Tephritidae, Muscidae, Calliphoridae, and Drosophilidae have separated millions of years ago.…”

“…Very similarly, Zaprionus indianus and Z. camerounensis that are also distantly related to the Sophophora subgenus, but restricted to tropic regions, exhibit a CRY/PDF expression pattern that is undistinguishable from D. melanogaster (Figure b) (Beauchamp et al., ). Even subtropic species outside the Drosophilidae such as olive flies, B. oleae (Diptera: Tephritidae), have a clock network that strongly resembled that of D. melanogaster (Bertolini et al., ). Together, these results strongly suggest that the D. melanogaster ‐like clock network is the ancestral one that is preserved in all fly species that did not invade high latitudes.…”

“…Thus, the adaptation of the daily activity patterns to different environmental conditions can be easily observed in flies, although individual animals are relatively short‐lived and do usually not experience several seasons (only the individuals that overwinter experience autumn, winter, and spring). The great advantage of studying flies is that the molecular and neuronal mechanisms of the circadian clock are well‐understood in D. melanogaster (see King & Sehgal, this issue) and start to emerge also in other Diptera (Bazalova & Dolezel, ; Bertolini et al., ; Codd et al., ; Gentile, Rivas, Meireles‐Filho, Lima, & Peixoto, ; Gesto et al., ; Kaiser et al., ; Kyriacou, ; Meireles‐Filho & Kyriacou, ; Meuti, Stone, Ikeno, & Denlinger, ; Noreen, Pegoraro, Nouroz, Tauber, & Kyriacou, ; Rivas et al., ; Rund, Hou, Ward, Collins, & Duffield, ). In D. melanogaster , recent studies have shown that M and E activity bouts are reflected by Ca 2+ rhythms in the relevant clock neurons controlling M and E activity, respectively (Liang, Holy, & Taghert, , ).…”

Identification and synthesis of new sex-specific components of olive fruit fly (Bactrocera oleae) female rectal gland, through original Negishi reactions on supported catalysts

“…1 This invasive pest, widely known in the Mediterranean region, threated California olive crops as well. 2 The substantial economic impact of the damage losses of fruits and oil quality is dealt adopting different strategies, like insecticide-based control (e.g., dimethoate and fenthion), 3 biological control using natural enemies, 4 sterile insect techniques, 5 attraction to baits 6 lured with colors 7 and pheromones. 8 A pesticide-free approach would be of course the most appealing, for many reasons, including the risk for human and environmental health, not to --- Corresponding authors.…”