Review
Insecticide resistance in Tephritid flies

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Abstract

Tephritid flies attack a large variety of fruits, which constitute highly-priced commodities in many countries. Insecticides have been used extensively for their control.

Although resistance development in fruit flies has not kept pace with that in other insects, possibly due to their high mobility and tendency for wide spatial dispersal, recent studies have indicated that selection pressure has now reached the point where resistance is detectable in the field and control may therefore become problematic. The status of resistance to the commonly used insecticides in the most significant Tephritid pests, such as the Mediterranean fruit fly Ceratitis capitata, the oriental fruit fly Bactrocera dorsalis, the olive fly Bactrocera oleae and the melon fly Bactrocera cucurbitae, is reviewed. Emphasis has been placed on the resistance mechanisms that have been elucidated at the biochemical and molecular level. Prospects for using this knowledge alongside genomic information in Tephritidae to develop novel strategies of potential practical importance for resistance management are discussed.

Highlights

Insecticide resistance status of Tephritidae flies. ► Review of insecticide resistance mechanisms in Tephritidae flies. ► Comparative genomic information in Tephritidae to develop novel control strategies.

Introduction

The family Tephritidae is a group of poly-phytophagous flies which contain some of the most damaging fruit pests in the world. As of December 2003, it included 4448 known species arranged in 484 genera (Norrbom, The Diptera Site – http://www.sel.barc.usda.gov/diptera/tephriti/TephClas.htm). Among them, the Mediterranean fruit fly (medfly) Ceratitis capitata (Wiedemann), which causes extensive damage to citrus orchards, is classified as the most significant pest [1]. Other pests include the oriental fruit fly Bactrocera dorsalis (Hendel), of great economic importance in the Asia-Pacific region, the olive fly Bactrocera oleae (Rossi), the most destructive pest of olive trees, the Queensland fruit fly B. tryoni (Froggatt), the melon fly Bactrocera cucurbitae (Coquillett), the lesser pumpkin fly Dacus ciliatus (Loew), the apple maggot fly Rhagoletis pomonella (Walsh), the cherry fruit fly R. cerasi (L.), and the Mexican and Caribbean fruit flies Anastrepha ludens (Loew) and A. suspensa (Loew), respectively.

Although sterile insect release (SIT), mass trapping and mating disruption technologies have been employed extensively to manage Tephritid fruit flies, use of chemicals has been a principal tool in many control practices worldwide [1]. The use of bait and cover sprays are the most common application strategies.

Organochlorines (OCLs), organophosphates (OPs) and carbamates (CARBs) were initially used to control Tephritid flies, followed by the more recent introduction of pyrethroids, spinosad and other compounds.

Before 1990, despite heavy exposure to insecticides, fruit flies had shown no clear evidence of resistance under practical field conditions [2], [3], [4].

Among the factors that may have a delaying effect on the evolution of resistance in fruit flies, are their high mobility and the tendency for wide spatial dispersal, both characteristics enabling the populations to rapidly move to alternative hosts, thus escaping continuous exposure to chemical [5]. However, recent reports have indicated that selection pressure has resulted in the development of resistance which in turn is becoming a problem for effective control (Table 1).

Resistance to insecticides has been attributed to mutations in the insecticide targets which reduce their sensitivity to the toxic molecule, or to increased rates of insecticide detoxification, which compromises the effective dosage of the insecticide that reaches the target. Reduced insecticide penetration by a thickening or a change in the chemical composition of the cuticle or altered behaviour so that insect avoids exposure to insecticides can also contribute to resistance. Knowledge of the underlying molecular mechanisms associated with insecticide resistance is relatively limited in Tephritid flies. Modified acetylcholinesterase (MACE) – based OP resistance has been studied extensively in B. oleae [6], [7], B. dorsalis [8], [9] and C. capitata [10] and specific mutations responsible for the phenotype have been identified. Target site resistance to pyrethroids and spinosad has been indicated in some Tephritidae species, but no specific resistance mutations have been identified as yet [11], [12], [13].

The implication of enzyme families known to be involved in insecticide detoxification, such as carboxyesterases (COEs) [14], glutathione S-transferases (GSTs) [15] and P450 mixed function oxidases (MFOs) [16] have been less well studied in Tephritid flies. COEs have been associated with B. oleae and C. capitata OP resistance [10], [17], while elevated MFOs have been associated with pyrethroid resistance in B. oleae [13] and B. dorsalis [11].

Today the major emphasis of insecticide resistance research is placed on the elucidation of underlying molecular mechanisms and the identification of specific changes at the genomic DNA level associated with the trait, aiming to use this information for the subsequent development of molecular diagnostics, which are essential tools in resistance management.

Here insecticide resistance in Tephritid flies is reviewed with emphasis placed on the biochemical and molecular mechanisms underlying resistance that have been characterised to date. How this knowledge can be used alongside available genomic information for Tephritidae in regards to improving current control strategies is discussed.

Section snippets

Bioassay data

OPs and CARBs are widely used to control a broad range of arthropod pests of agricultural and medical importance, including Tephritid fruit flies. OPs and CARBs that have been used most frequently in fruit fly control include dimethoate, fenthion, naled, malathion, fenitrothion, formothion (OPs), and methomyl (CARB).

The first OP resistance studies in Tephritid flies were carried out in the olive fruit fly B. oleae [18], [19] a pest that has been subjected to selection pressure by dimethoate and

Bioassay data

Pyrethroids, such as deltamethrin, alpha-cypermethrin, fenvalarate, lambda-cyhalotrin and cyfluthrin, have been used extensively for the control of Tephritid fruit flies. However, a limited number of pyrethroid resistance cases have been documented in the literature (Table 1).

In the earliest study, Busch-Petersen and Wood [36] reported moderate levels of permethrin resistance (up 20-fold) in C. capitata from Israel after laboratory selection. More recently, a 42-fold lambda-cyhalothrin

Bioassay data

Spinosad is derived from the bacteria Saccharopolyspora spinosa and has efficacy against a wide range of insects. It has been used extensively for the control of several fruit flies [40], [41], [42].

Low levels of spinosad resistance (4–13-fold) were detected in field populations of B. oleae from California, where the active ingredient has been used for about 10 years (bait applications), while resistance was not detected in field populations from Greece [43]. However, low levels of Spinosad

Resistance to other insecticide classes

The potential for organoclorine (OCL) resistance in medflies was studied in the early 1980’s with the main objective of developing a genetic sexing mechanism for the implementation of SIT in fruit fly control [46]. Two review articles have already described these results [2], [4], which are summarised in Table 1. A low potential for the selection of DDT, dieldrin and lindane resistance was reported. Similar levels of resistance were acquired in the melon fruit fly B. cucurbitae against lindane

Comparative Tephritidae genomics for resistance studies

Similar life cycles of Tephritids are reflected in the similarity of their genomes which, in turn, respond similarly to environmental challenges. Among these challenges is the exposure to insecticides that often cause analogous changes to the species genetic material. In that regard, the study of one Tephritid fly may provide valuable information in the resistance developed in a different species. This genomic similarity comes from several lines of evidence. Firstly, phylogenetic studies based

Discussion and conclusions

The status of resistance to commonly used insecticides in the most significant pests among Tephritid flies has been reviewed here. Relatively moderate resistance levels have been recorded in the field, if one considers the frequency, duration and intensity of the chemical control interventions, particularly for C. capitata, B. oleae, B. dorsalis and B. curcubitae. The majority of resistance cases refer to phenotypes obtained after laboratory selection (Table 1), which only serve as indicators

Acknowledgments

Work performed by John Vontas was supported from funds received by the Greek Ministry of Rural Development and Food. Work performed by Félix Ortego and Pedro Hernández-Crespo is receiving financial support from the Spanish Ministry of Science and Innovation (AGL2007-63388/AGR).

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