Mate choice by wild and mass‐reared females of the Mediterranean fruit fly

The sterile insect technique (SIT) is used to control Mediterranean fruit fly, Ceratitis capitata (Wiedemann), but its effectiveness is limited by low sexual competitiveness of mass‐reared males. This study investigated whether wild and mass‐reared [from a temperature sensitive lethal (tsl) genetic sexing strain] females display similar mate preferences and thus exert similar selective forces on the evolution of male courtship behaviour. Wild females preferred wild males over tsl males, whereas tsl females mated indiscriminately. The probability that mounting resulted in copulation was related to the duration of pre‐mount courtship for wild females, and wild males performed longer courtships than tsl males. Copulation occurred independently of courtship duration in tsl females. Counter to the aim of the SIT, female choice by tsl females appears to promote the evolution of male behaviour disfavoured by wild females.     

Aromatherapy on a large scale: exposing entire adult holding rooms to ginger root oil increases the mating competitiveness of sterile males of the Mediterranean fruit fly in field cage trials

The sterile insect technique (SIT) is widely used in integrated programs against fruit fly pests, particularly the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Unfortunately, the mass-rearing procedures inherent to the SIT often lead to a reduction in male mating competitiveness. One potential solution involves the pre-release exposure of males to specific attractants. In particular, male exposure to ginger root oil [Zingiber officinale Roscoe (Zingiberaceae); hereafter GRO] has been shown to increase mating success dramatically in field cage trials. Initial studies exposed small groups of males (25 individuals), but more recent work has demonstrated that GRO exposure involving standard storage boxes (containing ≈ 36 000 males) also results in enhanced mating performance. The objective of the present study was to determine whether aromatization of entire trailers, holding ≈ 14 million sterile males from a genetic sexing [temperature sensitive lethal (tsl)] strain, increases male mating success. Independent of the total dose, spatial distribution, or type of dispenser used, sterile males exposed to GRO for a 24-h period displayed greater mating success than non-exposed males in mating cage trials (in which tsl males competed against males from a standard, bisexual strain for females from this same standard strain). Averaged over all experiments, tsl males exposed to GRO obtained 54% of all matings compared to 38% for non-exposed tsl males, an increase of 42%. The implications of these findings for SIT programs against C. capitata are discussed.     

Genetics‐based methods for agricultural insect pest management

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Transgenic sexing system for Ceratitis capitata (Diptera: Tephritidae) based on female-specific embryonic lethality

Fruit fly pest species have been successfully controlled and managed via the Sterile Insect Technique (SIT), a control strategy that uses infertile matings of sterile males to wild females to reduce pest populations. Biological efficiency in the field is higher if only sterile males are released in SIT programs and production costs are also reduced. Sexing strains developed in the Mediterranean fruit fly Ceratitis capitata (medfly) through classical genetics are immensely beneficial to medfly SIT programs but exhibit reduced fertility and fitness. Moreover, transfer of such classical genetic systems to other tephritid species is difficult. Transgenic approaches can overcome this limitation of classical genetic sexing strains (GSSs), but had resulted so far in transgenic sexing strains (TSSs) with dominant lethality at late larval and pupal stages. Here we present a transgene-based female-specific lethality system for early embryonic sexing in medfly. The system utilizes the sex-specifically spliced transformer intron to restrict ectopic mRNA translation of the pro-apoptotic gene hid^Ala5 to females only. The expression of this lethal effector gene is driven by a tetracycline-repressible transactivator gene tTA that is under the control of promoters/enhancers of early-acting cellularization genes. Despite observed position effects on the sex-specific splicing, we could effectively establish this early-acting transgenic sexing system in the medfly C. capitata. After satisfactory performance in large scale tests, TSSs based on this system will offer cost-effective sexing once introduced into SIT programs. Moreover, this approach is straight forward to be developed also for other insect pest and vector species.     

Population Genetics of Ceratitis capitata in South Africa: Implications for Dispersal and Pest Management

The invasive Mediterranean fruit fly (medfly), Ceratitis capitata, is one of the major agricultural and economical pests globally. Understanding invasion risk and mitigation of medfly in agricultural landscapes requires knowledge of its population structure and dispersal patterns. Here, estimates of dispersal ability are provided in medfly from South Africa at three spatial scales using molecular approaches. Individuals were genotyped at 11 polymorphic microsatellite loci and a subset of individuals were also sequenced for the mitochondrial cytochrome oxidase subunit I gene. Our results show that South African medfly populations are generally characterized by high levels of genetic diversity and limited population differentiation at all spatial scales. This suggests high levels of gene flow among sampling locations. However, natural dispersal in C. capitata has been shown to rarely exceed 10 km. Therefore, documented levels of high gene flow in the present study, even between distant populations (>1600 km), are likely the result of human-mediated dispersal or at least some form of long-distance jump dispersal. These findings may have broad applicability to other global fruit production areas and have significant implications for ongoing pest management practices, such as the sterile insect technique.     

Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae)

Background  

The sterile insect technique (SIT) is an environment-friendly method used in area-wide pest management of the Mediterranean fruit fly Ceratitis capitata (Wiedemann; Diptera: Tephritidae). Ionizing radiation used to generate reproductive sterility in the mass-reared populations before release leads to reduction of competitiveness.     

The effects of sterile males and two braconid parasitoids,Fopius arisanus (Sonan) and Diachasmimorpha krausii (Fullaway) (Hymenoptera), on caged populations of Mediterranean fruit flies,Ceratitis capitata (Wied.) (Diptera: Tephritidae) at various sites in Guatemala

Area-wide control of the Mediterranean fruit fly (=medfly), Ceratitis capitata (Wiedemann), typically involves sterile insect technique (=SIT), and at present the “Temperature Sensitive Lethal” (=TSL) strain is commonly mass-reared for such releases. In theory, and with some experimental support, the augmentative addition of parasitoids to sterile releases can suppress pest populations to a greater extent than either technique alone. The efficacies of TSL males, parasitoids, and TSL males and parasitoids were compared in large field cages erected over coffee grown at four locations and three altitudes (relatively high, medium and low for the crop) in Guatemala. Two species of opiine braconid parasitoids, the larval–pupal parasitoid Diachasmimorpha krausii (Fullaway) and the egg-pupal parasitoid Fopius arisanus (Sonan), were released either together or in combination with sterile males into cages along with fertile medflies. Results of this evaluation were assessed by comparing the number of pupae and adult insects that completed development (F1 generation) as a result of the reproduction of a parental generation released into each field cage. The TSL males significantly suppressed F1 fly populations but only in one of four study sites. However, the inclusion of F. arisanus and D. krausii always provided significant suppression and the effect was frequently substantial. In one site there was a significant interaction between the capacity of sterile males and parasitoids to suppress caged fly populations. There was no effect of host-fruit abundance on the numbers of flies recovered, however, there were significant interactions between maximum and minimum temperatures and the effects of sterile males and parasitoids, respectively. The results suggest that mass-reared sterile medflies and biological control agents should be tested for both consistent sexual-quality and their ability to perform in the various environments in which they will be released.     

Genetics and biology of <Emphasis Type="Italic">Anastrepha fraterculus</Emphasis>: research supporting the use of the sterile insect technique (SIT) to control this pest in Argentina

Two species of true fruit flies (taxonomic family Tephritidae) are considered pests of fruit and vegetable production in Argentina: the cosmopolitan Mediterranean fruit fly (Ceratitis capitata Wiedemann) and the new world South American fruit fly (Anastrepha fraterculus Wiedemann). The distribution of these two species in Argentina overlaps north of the capital, Buenos Aires. Regarding the control of these two pests, the varied geographical fruit producing regions in Argentina are in different fly control situations. One part is under a programme using the sterile insect technique (SIT) for the eradication of C. capitata, because A. fraterculus is not present in this area. The application of the SIT to control C. capitata north of the present line with the possibility of A. fraterculus occupying the niche left vacant by C. capitata becomes a cause of much concern. Only initial steps have been taken to investigate the genetics and biology of A. fraterculus. Consequently, only fragmentary information has been recorded in the literature regarding the use of SIT to control this species. For these reasons, the research to develop a SIT protocol to control A. fraterculus is greatly needed. In recent years, research groups have been building a network in Argentina in order to address particular aspects of the development of the SIT for Anastrepha fraterculus. The problems being addressed by these groups include improvement of artificial diets, facilitation of insect mass rearing, radiation doses and conditions for insect sterilisation, basic knowledge supporting the development of males-only strains, reduction of male maturation time to facilitate releases, identification and isolation of chemical communication signals, and a good deal of population genetic studies. This paper is the product of a concerted effort to gather all this knowledge scattered in numerous and often hard-to-access reports and papers and summarize their basic conclusions in a single publication.     

Riding the Trojan horse: combating pest insects with their own symbionts

Insects form an extremely large group of animals and bear a consequently large variety of associated microbes. This microbiota includes very specific and obligate symbionts that provide essential functions to the host, and facultative partners that are not necessarily required for survival. The Tephritidae is a large family that includes many fruit pests such as the Mediterranean fruit fly (the medfly, Ceratitis capitata) and the Olive fly (Bactrocera oleae). Community and functional analyses showed that the microbiota of both flies contribute to their diet, and affect host fitness parameters. The analysis of the microbiota's community structure of mass‐reared, sterilized medfly males used in the sterile insect technique revealed a strong reduction in Klebsiella spp. compared with non‐sterile and wild flies. Inoculation of sterile males with this gut population affected female mating behaviour as they preferentially mated with inoculated versus non‐inoculated males. These studies suggest that control can be significantly improved by manipulating symbionts in pest animals.     

Sterile males of Ceratitis capitata (Diptera: Tephritidae) as disseminators of Beauveria bassiana conidia for IPM strategies

Sterile Mediterranean fruit fly, Ceratitis capitata (Wied.), males were evaluated as vectors to spread Beauveria bassiana (Bals) conidia to wild C. capitata populations under field conditions. The inoculated sterile males were released by air, using the chilled adult technique over 7000 ha of coffee growing in Chimaltenango, Guatemala, Central America. The impact of releases was determined using dry traps baited with a food attractant. The effects of these releases on Apis mellifera, Linnaeus (honey bee), Hypothenemus hampei, Ferrari (coffee berry borer) and the parasitic mite Varroa destructor (Oudeman) were also evaluated. Inoculated sterile males were able to transmit fungal spores to 44% of the wild C. capitata flies captured in traps, which likely were infected through intra- and intersexual interactions during leks, mating or mating attempts. There was no transmission of the fungal spores to non-target insect species such as coffee berry borer, honey bees or varroa. We conclude that sterile males of Mediterranean fruit fly inoculated with B. bassiana can act as effective vectors of conidia to wild populations, constituting a safe, environmentally friendly and selective alternative for suppressing the medfly under a Sterile Insect Technique-based IPM approach.     

Mass rearing of temperature sensitive genetic sexing strains in the Mediterranean fruit fly (Ceratitis capitata)

Genetic sexing strains (GSS) based on the temperature sensitive lethal(tsl) mutation are being used to produce sterile male medflies for large scale sterile insect technique (SIT) programmes for this pest. The use of male-only strains increases the overall efficiency of the technique. Currently more than 1.4 billion sterile male-only pupae are produced per week in different facilities around the world. Due to the mutations used to construct these strains, that is, translocations and selectable markers, they require different and more careful mass rearing procedures than do bisexual strains (BSS). The basic rearing technology has been developed and can be used to produce only males on a predictable basis to a level of 99.9% accuracy. If specific rearing procedures are followed, then tsl-based GSS has a rearing efficiency that is equal to that of a BSS and it is already know that males produced by the tsl-based GSS are of equal quality to males produced by BSS. Based on current rearing technology the cost of production of male pupae is about the same for both types of strain. This is due to the large colony that is required for the tsl-based GSS. This paper discusses the considerations that need to be taken into account during mass rearing of GSS and identifies the most efficient production processes that are currently available.     

Genetic elimination of field-cage populations of Mediterranean fruit flies

The Mediterranean fruit fly (medfly, Ceratitis capitata Wiedemann) is a pest of over 300 fruits, vegetables and nuts. The sterile insect technique (SIT) is a control measure used to reduce the reproductive potential of populations through the mass release of sterilized male insects that mate with wild females. However, SIT flies can display poor field performance, due to the effects of mass-rearing and of the irradiation process used for sterilization. The development of female-lethal RIDL (release of insects carrying a dominant lethal) strains for medfly can overcome many of the problems of SIT associated with irradiation. Here, we present life-history characterizations for two medfly RIDL strains, OX3864A and OX3647Q. Our results show (i) full functionality of RIDL, (ii) equivalency of RIDL and wild-type strains for life-history characteristics, and (iii) a high level of sexual competitiveness against both wild-type and wild-derived males. We also present the first proof-of-principle experiment on the use of RIDL to eliminate medfly populations. Weekly releases of OX3864A males into stable populations of wild-type medfly caused a successive decline in numbers, leading to eradication. The results show that genetic control can provide an effective alternative to SIT for the control of pest insects.     

The putative‐farnesoic acid O‐methyl transferase (FAMeT) gene of Ceratitis capitata: characterization and pre‐imaginal life expression

Farnesoic acid O‐methyl transferase (FAMeT) is the enzyme involved in the penultimate step of insect juvenile hormone (JH) biosynthesis and is thus a key regulator in insect development and reproduction. We report the characterization of the putative‐FAMeT in the medfly or Mediterranean fruit fly, Ceratitis capitata. This gene was identified by suppressive subtractive hybridization and completely sequenced by the screening of a medfly cDNA library. The obtained sequence was analyzed for conserved protein domain identification and its expression profile was evaluated by quantitative Real‐Time PCR in medfly pre‐imaginal life. The tissue expression of the isolated gene was verified by in situ hybridization on third instar larvae sections. The characterization of the isolated gene pointed out several typical features of methyl transferase genes. The pre‐imaginal putative‐FAMeT expression levels were consistent with JH titer change in Diptera. As recognized in some crustaceans, this gene seems to be widely expressed in the medfly as well. Ceratitis capitata is one of the most relevant agricultural pests against which insecticides and the sterile insect technique (SIT) are extensively used in spite of the well‐known limitations of these approaches. Although results are not conclusive for the physiological role of the isolated gene, they suggest the characterization of a new gene in the Mediterranean fruit fly potentially involved in JH biosynthesis and may, therefore, have implications for pest control. © 2010 Wiley Periodicals, Inc.     

Pathogenicity of Beauveria bassiana isolated from Moroccan Argan forests soil against larvae of Ceratitis capitata (Diptera: Tephritidae) in laboratory conditions

The Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae), is the major tephritid pest in Morocco. This pest survives in Moroccan forests Argania spinosa and continually invades the nearest agricultural areas. Entomopathogenic fungi are an interesting tool for fruit fly control and hold a useful alternative to conventional insecticides. However, primary selection of effective pathogens should be taken in laboratory condition prior to applying them in the field. Here, we used third late instar larvae of C. capitata to investigate the effectiveness of 15 local Beauveria bassiana isolates. Results showed that all isolates were able to infect the larval stage, producing a large mortality rate in puparia ranging from 65 to 95 % and caused significant reduction in adult emergence. The fungal treatments revealed that the mycosis occurred also in adults escaping infection as pupariating larvae. The percentage of mycosed puparia was highest in strain TAM6.2 (95 %) followed by ERS4.16 (90 %), therefore they were the most virulent. Median lethal concentration (LC₅₀) was studied for five isolates at four concentrations ranging from 10⁵ to 10⁸ conidia ml^?1. The results showed that the slopes of regression lines for B. bassiana ERS4.16 (slope = 0.386) and TAM6.2 (slope = 0.41) were the most important and had the lowest LC₅₀ values (2.85 × 10³ and 3.16 × 10³ conidia ml^?1 respectively). This investigation suggests that the soil of Argan forests contains pathogenic B. bassiana isolates and highlights for the first time their potential as biological control toward C. capitata larval stage in Morocco.     

The Significance of Genetic Polymorphisms within and between Founder Populations of Ceratitis capitata (Wied.) from Argentina

Background

The Mediterranean fruit fly Ceratitis Capitata (DIPTERA: Tephritidae) is a major agricultural pest in Argentina. One main cause for the success of non-contaminant control programs based on genetic strategies is compatibility between natural and laboratory germplasms.A comprehensive characterization of the fruit fly based on genetic studies and compatibility analysis was undertaken on two founder populations from the provinces of Buenos Aires and Mendoza, used in pioneering sterile male technique control programmes in our country. The locations are 1,000 km apart from each other.

Methodology/Principal Findings

We compared the genetic composition of both populations based on cytological, physiological and morphological characterization. Compatibility studies were performed in order to determine the presence of isolation barriers. Results indicate that the Buenos Aires germplasm described previously is partially different from that of the Mendoza population. Both laboratory colonies are a reservoir of mutational and cytological polymorphisms. Some sexual chromosome variants such as the XL and the YL resulting from attachment of a B-chromosome to the X-chromosome or Y-chromosome behave as a lethal sex-linked factor. Our results also show incompatibility between both germplasms and pre-zygotic isolation barriers between them. Our evidence is consistent with the fact that polymorphisms are responsible for the lack of compatibility.

Conclusions

The genetic control mechanism should be directly produced in the germplasm of the target population in order to favour mating conditions. This is an additional requirement for the biological as well as economic success of control programs based on genetic strategies such as the sterile insect technique. The analysis of representative samples also revealed natural auto-control mechanisms which could be used in modifying pest population dynamics.     

Temperature effects on “overwintering” phenology of a polyphagous,tropical fruit fly (Tephritidae) at the subtropical/temperate interface

Around the world, several pest tephritids are extending their ranges from warm tropical or Mediterranean climates into cooler temperate regions. The ability to tolerate climatic diversity is uncommon among insects, and understanding the population phenology drivers of such species across different parts of their range will be critical for their management. Here, we determined the role of temperature versus fruit availability on the population phenology of Queensland fruit fly, Bactrocera tryoni. Using a field site located at the subtropical/temperate interface, with host fruits continuously available, we monitored the development times and abundance of B. tryoni, a species which has invaded temperate Australia from the tropics. From fruit samples held at ambient and controlled conditions, the abundance of emerging flies was highly variable among collection dates, but the variance did not reflect the observed changes in temperature. For most samples, the survival rate of flies in a field site was lower than predicted by a day‐degree population model fitted with mean daily field temperatures. The development time of the immature stage in the field was prolonged, presumably due to cooler ambient conditions, but the fitted day‐degree population model consistently over‐predicted estimated development times. Our results indicate that at the subtropical/temperate interface, the decline in B. tryoni populations during winter is only partly driven by temperature and host availability. We classify B. tryoni as a climate generalist, which likely employs physiological as well as behavioural mechanisms to achieve broad climatic tolerance ranges.     

Identification and biochemical characterisation of α-amylase in the alimentary tract of Mediterranean fruit fly,Ceratitis capitata (Wiedemann) (Diptera: Tephritidae)

Mediterranean fruit fly (Medfly), Ceratitis capitata, is an important pest of many fruit crops in temperate and subtropical regions worldwide. α-Amylases are hydrolytic enzymes involved in carbohydrate metabolism in insects. There is no report about α-amylase activity in C. capitata in literature. So, the aim of the current study was biochemical characterisation of α-amylase in the alimentary canal of the pest to gain a better understanding of digestive physiology of the insect. α-Amylase of Medfly was extracted and characterised using starch as the substrate. The results showed the presence of α-amylase activity in the gut of the insect for carbohydrate digestion. Optimum activity of the enzyme occurs at pH 8.0 and 40?°C. The most effective activator of the enzyme was determined in treatment with 20?mM CaCl₂. Na⁺, K⁺ and Mg²⁺ ions also activated the enzyme. Native PAGE of α-amylase showed two isoenzymes suggesting the importance of α-amylase in the carbohydrate digestion in the insect. Understanding of the digestive physiology and α-amylase activity of Medfly is important when new management strategies for this economically important pest are devised.     

Comparative demography of three neotropical larval-prepupal parasitoid species associated with Anastrepha fraterculus (Diptera: Tephritidae)

The South American fruit fly, Anastrepha fraterculus (Wiedemann), is one of two fruit fly species of economic importance in Argentina, which along with the exotic Mediterranean fruit fly, Ceratitis capitata (Wiedemann) produce annual losses of nearly US$ 90 million for fruit production in this country.Biological control may contribute to integrated approaches to manage both pestiferous species.Information on survival, reproduction and population growth parameters, critical for successful augmentation of natural enemies, is provided for three fruit fly neotropical parasitoids, Aganaspis pelleranoi (Hymenoptera: Figitidae), Opius bellus and Doryctobracon crawfordi (Hymenoptera: Braconidae). A. pelleranoi had the highest intrinsic reproductive rate (r), survival time and reproductive time, followed by O. bellus. Meanwhile D. crawfordi showed the lowest values for reproductive and population growth parameters.