Genetic and cytogenetic analysis of the American cherry fruit fly, Rhagoletis cingulata (Diptera: Tephritidae)

The American eastern cherry fruit fly, Rhagoletis cingulata, a pest of cherries in the western hemisphere, invaded Europe in 1983, and since then dispersed to several European countries. Information on the genetics and cytogenetics of this pest is very scarce. The mitotic karyotype and detailed photographic maps of the salivary gland polytene chromosomes of R. cingulata are presented here. The mitotic metaphase complement consists of six pairs of chromosomes with the sex chromosomes being very small and similar in size. The analysis of the salivary gland polytene complement shows a total number of five long chromosomes (10 polytene arms), which correspond to the five autosomes of the mitotic nuclei and an extrachromosomal heterochromatic mass, which corresponds to the sex chromosomes. The banding patterns and the most characteristic features and prominent landmarks of each polytene chromosome are presented and discussed. Chromosomal homologies between R. cingulata, R. completa and R. cerasi are also proposed, based on the comparison of chromosome banding patterns. Furthermore, the detection and characterization of Wolbachia pipientis in the R. cingulata population studied is presented and the potential correlation with the asynaptic phenomena found in its polytene complement is discussed. In addition, 10 out of 24 microsatellite markers developed for other Rhagoletis species are cross-amplified, evaluated and proposed as useful markers for population and genetic studies in R. cingulata.     

Genetic and cytogenetic analysis of the olive fruit fly Bactrocera oleae (Diptera: Tephritidae)

The genetic and cytogenetic characteristics of one of the major agricultural pests, the olive fruit fly Bactrocera oleae, are presented here. The mitotic metaphase complement of this insect consists of six pairs of chromosomes including one pair of heteromorphic sex chromosomes, with the male being the heterogametic sex. The analysis of the polytene complements of three larval tissues, the fat body, the salivary glands and the Malpighian tubules of this pest has shown (a) a total number of five long chromosomes (10 polytene arms) that correspond to the five autosomes of the mitotic nuclei and a heterochromatic mass corresponding to the sex chromosomes, (b) the constancy of the banding pattern of the three somatic tissues, (c) the absence of a typical chromocenter as an accumulation of heterochromatin, (d) the existence of reverse tandem duplications, and (e) the presence of toroid tips of the chromosome arms. The in situhybridization of genes or DNA sequences to the salivary gland polytene chromosomes of B. oleaeprovided molecular markers for all five autosomes and permitted the establishment of chromosomal homologies among B. olea, B. tryoniand Ceratitis capitata. The heat shock response of B. oleae, as revealed by heat-inducible puffing and protein pattern, shows a higher thermotolerance than Drosophila melanogaster.     

Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae)

The European cherry fruit fly Rhagoletis cerasi has been a field model for cytoplasmic incompatibility since the mid 1970s. Two Wolbachia strains were detected in this tephritid species and w Cer2 was described as the CI inducing agent dividing European populations into two unidirectional incompatible groups, i.e. southern females produce viable offspring with northern males, whereas the reciprocal cross results in incompatibility. We detected three new Wolbachia strains by sequencing a multitude of plasmids derived from Wolbachia surface protein gene ( wsp ) polymerase chain reaction (PCR) products. Strain-specific primers were developed allowing individual diagnosis without need for cloning. Hybridization of specific PCR products with a wsp oligonucleotide enhanced the detection limit significantly and revealed the presence of low-titre infections in some strains, in different ontogenetic stages and in adults of different age. We then performed a survey of strain prevalence and infection frequency in eight European regions. w Cer1 was fixed in all populations, whereas w Cer2 was detected only in the South. w Cer3 frequency was the lowest without a clear distribution pattern. The abundance of w Cer4 was homogenous across Europe. Like w Cer2, w Cer5 showed significant differences in spatial distribution. Our new findings of previously undetected and recombinant Wolbachia strains in R. cerasi reveal a major caveat to the research community not to overlook hidden Wolbachia diversity in field populations. Low-titres and geographical variability in Wolbachia diversity are expected to influence the outcome of Wolbachia population dynamics and Wolbachia- based insect population control and may create invasion barriers for expanding and artificially introduced Wolbachia strains.     

Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera,Tephritidae)

Wolbachia is an obligately intracellular, maternally inherited bacterium which has been detected in many arthropods. Wolbachia infections disperse in host populations by mechanisms such as cytoplasmic incompatibility (CI). CI leads to embryonic mortality which occurs when infected males mate with uninfected females or females with a different Wolbachia strain. Populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae) were found to be infected by two different Wolbachia strains, wCer1 and wCer2. Superinfections with both strains occurred throughout southern and central Europe and infections with wCer1 were found in northern, western and eastern Europe. Strong unidirectional CI between European populations of R. cerasi were first reported in the 1970s. From the conformity in the recent geographical distribution of the Wolbachia infections and the CI expression patterns found 25 years ago it was deduced that wCer2 potentially causes CI in R. cerasi. The comparison of the geographical distributions indicated that wCer1 + 2 must have spread into wCer1-infected populations in some areas. In other regions, a spread of wCer1 + 2 was probably prevented by dispersal barriers. There, a sharp transition from infected to superinfected populations suggested regional isolation between wCer1 and wCer1 + 2-infected populations.     

Evaluation of trap types and food attractants for Rhagoletis cerasi (Diptera: Tephritidae)

Trapping experiments were conducted during the period of flight activity of the cherry fruit fly Rhagoletis cerasi L. in the area of Thessaloniki, northern Greece, during the years 1993-1997 to test several traps alone and in combination with different food attractants. Yellow sticky-coated visual traps were more effective than McPhail-type traps baited with different food attractants. Of the visual traps, the most effective was the yellow Rebell trap. The Rebell trap, provided with a dispenser containing a slow release formulation of ammonium acetate attached to the lower part of the trap, was found to be the most effective of all treatments tested, capturing approximately 50% more R. cerasi flies than the Rebell trap without any attractant. Ammonium carbonate dispensers did not increase the performance of Rebell traps. More mature females were captured in Rebell traps baited with or without ammonium acetate than in McPhail-type traps baited with ammonium acetate. This study demonstrates that Rebell traps baited with an ammonium acetate dispenser can provide a more effective tool for monitoring and mass trapping of R. cerasi than the currently used unbaited Rebell traps.     

Habitat-specific flight period in the cherry fruit fly Rhagoletis cingulata (Loew) (Diptera: Tephritidae)

Flight periods of the cherry fruit fly, Rhagoletis cingulata (Loew), were compared in the major sweet and tart cherry-growing regions of Michigan, among neglected orchards, managed orchards, and natural areas containing the ancestral host, black cherry. Traps were deployed from early June to late September 2005 and 2006. Captures indicated that cherry fruit fly has an early flight (June-July) in neglected orchards, a mid-season flight peaking immediately after harvest (June-August) in managed orchards, and an extended flight covering most of the season (June-September) in natural areas. We found that the period of fruit infestation mirrored the flight period in neglected and managed orchards. In natural areas, we found infestation late in the season only. The relative emergence periods for adults reared from pupae collected from the three habitats and maintained under the same conditions coincided with adult flight periods for each habitat. We also studied factors related to fruit availability that may have a role in shaping the flight periods. Fruit abundance decreased rapidly early in the season in neglected orchards, whereas in managed orchards, fruit left after harvest remained on the trees until late August. Measurements of fruit size and skin firmness revealed that fly activity in neglected and managed orchards began immediately after fruit increased in size and skin firmness decreased, whereas in natural areas, the flight began before fruit matured. In managed orchards, fruit harvest and insecticide sprays likely maintain the late flight period of resident fly populations by preventing the use of fruit earlier in the season. However, a significant proportion of these resident flies may still emerge before harvest and increase the risk of costly fruit infestation.     

Characterization of microsatellite loci for the western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae)

The western cherry fruit fly (Rhagoletis indifferens) is a major pest of cherry crops in western North America, yet relatively little is known about its population structure or movement patterns due to the difficulty of studying these parameters directly in the field. We isolated and characterized a set of 16 polymorphic microsatellite loci specific to R. indifferens that display sufficient polymorphism to assess genetic structure and movement patterns. All 16 loci amplified in one or more other Rhagoletis species, indicating that they are useful tools for genetic analysis in other members of the genus, many of which are also agricultural pests.     

Effect of altitude on seasonal flight activity of Rhagoletis cerasi flies (Diptera: Tephritidae)

The effect of altitudinal variation on the seasonal flight activity of Rhagoletis cerasi (Linnaeus) flies was evaluated along an altitudinal gradient from 150 to 1170 m in Mount Uludag, northwestern Turkey. The predicted dates of fly emergence, flight duration and dates of 5%, 50% and 95% cumulative fly catches at various altitudes were estimated from a degree-day model. Degree-day predictions were compared with those obtained from observations made with yellow sticky traps. The observed and predicted dates of appearance of adults were delayed by 1.4 and 2.0 days for every 100 m increase in altitude, respectively. The delay in phenology events was less at high altitudes than postulated by Hopkins' bioclimatic law, whether observed or predicted. The average absolute difference in predicted and observed dates of cumulative percentage catch of adults was 4.9 and 3.0 days in 1997 and 1998, respectively, but these differences were not significant. Prolonged flight activity was predicted and observed at higher altitudes, but the flight period lasted significantly longer than predicted. The observed flight period varied from 29 to 43 days in 1997 and from 36 to 52 days in 1998 between the lowest and highest altitude on the transect. Altitudinal variation between geographically close locations should be taken into account to properly time monitoring activities and hence to manage R. cerasi populations more effectively.     

Linkage analysis of five new genetic markers of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae).

Five new autosomal recessive genes are described in the oriental fruit fly, Bactrocera dorsalis (Hendel). These genetic markers are associated into three linkage groups. The matte (mt) gene is linked to the previously described mandarin red (ma) gene, and the white puparium (wp) gene is linked to the white eye (we) and amethyst (am) loci. The third designated linkage group has the yellow eye (ye) marker. The we/we homozygote is epistatic to ye/ye, and each is epistatic to am/am and ma/ma.     

Population genetic structure of the western cherry fruit fly Rhagoletis indifferens (Diptera: Tephritidae) in British Columbia,Canada

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Prolonged pupal dormancy is associated with significant fitness cost for adults of Rhagoletis cerasi (Diptera: Tephritidae)

In temperate areas, dormancy (diapause and/or quiescence) enables herbivorous insect species to persist and thrive by synchronizing growth and reproduction with the seasonal phenology of their host plants. Within-population variability in dormancy increases survival chances under unpredictable environmental changes. However, prolonged dormancy may be costly, incurring trade-offs in important adult fitness traits such as life span and reproduction. We used the European cherry fruit fly, Rhagoletis cerasi, a stenophagous, univoltine species that overwinters in the pupal stage for usually one or more years to test the hypotheses that prolonged dormancy of pupae has trade-offs with body size, survival and reproduction of the resulting adults. We used two geographically isolated populations of R. cerasi to compare the demographic traits of adults obtained from pupae subjected to one or two cycles of warm-cold periods (annual and prolonged dormancy respectively). Regardless of population, adults from pupae that experienced prolonged dormancy were larger than counterparts emerging within 1year. Prolonged dormancy did not affect adult longevity but both lifetime fecundity and oviposition were significantly decreased. Extension of the life cycle of some individuals in R. cerasi populations in association with prolonged dormancy is likely a bet-hedging strategy.     

Substantial progress made in the rearing of the European cherry fruit fly, Rhagoletis cerasi

We examined phenyl propionate as an attractant for trapping navel orangeworm, Amyelois transitella (Walker) (Lepidoptera: Pyralidae) adults, with the objective of developing a method of trapping both sexes more effectively than with almond meal. Two initial experiments maximized the total number of adults captured using phenyl propionate released from glass vials with cotton wicks. A third experiment compared the numbers of males and females captured using these glass dispensers in either bucket or sticky traps. The glass vial dispensers captured more adults than 0.1% phenyl propionate in water (as both attractant and killing agent), and far more adults were captured with glass vial phenyl propionate dispensers than with almond meal. On rare occasion, the glass vial dispensers captured as many adults as traps baited with virgin females, but usually phenyl propionate in glass vials captured fewer adults than virgin‐baited traps. Glass vial phenyl propionate dispensers were equally effective in sticky traps or bucket traps. The majority of females captured were mated, and the proportion of males captured increased over time within flights (generations). We conclude that phenyl propionate released from glass vials captured A. transitella adults more effectively than currently available options, and will be useful in research projects where capturing intact adults and comparing mating status are important. Developing a cost‐effective phenyl propionate‐based alternative to the egg traps currently used for commercial monitoring will be more difficult.     

The eggshell of the cherry fly Rhagoletis cerasi

One of the major pests in Greek cherry orchards is the cherry fly Rhagoletis cerasi (Diptera: Tephritidae). In order to complete our comparative work on the chorion assembly of other representatives of the fruit flies (e.g. Ceratitis capitata and Dacus oleae) we studied eggshell morphogenesis in the cherry fly. The oocyte is surrounded by several distinct layers which are produced during choriogenesis. The eggshell consists of the vitelline membrane, a fibrous layer of possible water-proofing function, an innermost chorionic layer, endochorionic and exochorionic layers. The endochorion shows a branched configuration with irregular cavities, and the exochorion consists of inner and outer layers for better embryo protection. At the anterior region of the follicle, the hexagonal borders of the follicle cells are created by endochorionic material, covered by both inner and outer exochorion. This area resembles the D. melanogaster chorionic appendages and therefore can serve for plastron respiration. The structural results support the phylogenetic relationships among the tephritids (Rhagoletis is closer to Ceratitis than Dacus). The presence of peroxidase in the endochorion, detected by diaminobenzidine, is consistent with the eggshell hardening at the end of choriogenesis, following the same pattern with the other fruit flies studied so far. Two major chorionic proteins are found both in R. cerasi and in C. capitata and therefore general conclusions can be drawn from this study, concerning the pattern of choriogenesis, which all dipteran insects follow, in order to create a resistant and functional eggshell, and the high conservation of the proteinaceous components of the chorion among species in the order.     

Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe

The widespread occurrence of Wolbachia in arthropods and nematodes suggests that this intracellular, maternally inherited endosymbiont has the ability to cross species boundaries. However, direct evidence for such a horizontal transmission of Wolbachia in nature is scarce. Here, we compare the well‐characterized Wolbachia infection of the European cherry fruit fly, Rhagoletis cerasi, with that of the North American eastern cherry fruit fly, Rhagoletis cingulata, recently introduced to Europe. Molecular genetic analysis of Wolbachia based on multilocus sequence typing and the Wolbachia surface protein wsp showed that all R. cingulata individuals are infected with wCin2 identical to wCer2 in R. cerasi. In contrast, wCin1, a strain identical to wCer1 in R. cerasi, was present in several European populations of R. cingulata, but not in any individual from the United States. Surveys of R. cingulata from Germany and Hungary indicated that in some populations, the frequency of wCin1 increased significantly in just a few years with at least two independent horizontal transmission events. This is corroborated by the analysis of the mitochondrial cytochrome oxidase II gene that showed association of wCin1 with two distinct haplotypes in Germany, one of which is also infected with wCin1 in Hungary. In summary, our study provides strong evidence for a very recent inter‐specific Wolbachia transmission with a subsequent spatial spread in field populations.     

Toxicological studies of organophosphate and pyrethroid insecticides for controlling the fruit fly Dacus ciliatus (Diptera: Tephritidae).

The fruit fly Dacus ciliatus Loew is a pest of the fruits of many cucurbit species. We studied the effect of organaophosphate and pyrethroid compounds on the adult flies by using surface contact and oral administration. In contrast to other fruit flies, we found that organophosphates were ineffective against D. ciliatus. This was supported by the insignificant decrease of head acetylcholinesterase activity. All tested pyrethroids showed satisfactory killing ability, rapid and massive knockdown effect, and prevention of oviposition. Piperonyl butoxide considerably increased the toxicity of pyrethroids, which can be explained by oxidase detoxification of these compounds in D. ciliatus. It can be concluded that pyrethroids have high potential for controlling D. ciliatus.     

Genetic delineation of sibling species of the pest fruit fly Bactocera (Diptera: Tephritidae) using microsatellites

Using a large set of microsatellites, the genetic relationships between three closely related Australian fruit fly species, Bactrocera tryoni (Froggatt), B. neohumeralis (Hardy) and B. aquilonis(May) were investigated. Bactrocera tryoni and B. neohumeralis are sympatric, while B. aquilonisis allopatric to both. The sympatric species, B. tryoni and B. neohumeralis, were found to be genetically distinct. It is likely that despite differences in mating time between these two species, some gene flow still occurs. In contrast, the sibling species B. tryoni and B. aquilonis were found to be closely related, despite allopatry. The level of genetic divergence was similar to that found within eastern Australian populations of B. tryoni. Consideration of all available genetic data suggests that this similarity is not due to recent (i.e. within the last 30 years) displacement of B. aquilonis by B. tryoni from the B. aquilonis region (north-western Australia). Instead the data suggests that, at least in the areas sampled, asymmetrical hybridization may have occurred over a longer timescale.     

Isolation and characterization of microsatellite loci from the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae)

We report the isolation and development of 81 novel primers for amplifying microsatellite loci in the Rhagoletis pomonella sibling species complex, and the sequencing, characterization and analysis of basic population genetic parameters for nine of these genes. We also report the successful cross‐species amplification of several of these loci. The R. pomonella sibling species complex is a textbook example of genetic differentiation in sympatry via host‐plant shifting. Microsatellite markers can be useful for mapping host‐plant‐associated adaptations in Rhagoletis that generate reproductive isolation and facilitate speciation, as well as for resolving the genetic structure and evolutionary history of fly populations.     

Revision of the fruit fly genus Capparimyia (Diptera, Tephritidae)

Capparimyia Bezzi is revised and eight species recognized, of which four are new: C. aenigma sp. nov., C. maerua sp. nov., C. mirabilis sp. nov., and C. spatulata sp. nov. A lectotype is designated for C. bipustulata (Bezzi, 1923), C. savastani (Martelli) and C. melanaspis (Bezzi). Capparimyia aristata nom. nov. is proposed as a replacement name for Pardalaspis (now Capparimyia ) bipustulata Bezzi, 1924 (preoccupied Bezzi, 1923). All species are described or re-described, with illustrations of mesonotal and wing patterns and male and female terminalia. A key to species is provided. Phylogenetic relationships within the genus are analysed cladistically and considered vis-à-vis the relationships between the host plants. Distribution patterns are discussed.     

Genetic consequences of domestication and mass rearing of pest fruit fly Bactrocera tryoni (Diptera: Tephritidae)

Tephritid fruit flies, an important pest of horticulture worldwide, are increasingly targeted for control or eradication by large-scale releases of sterile flies of the same species. For each species treated, strains must be domesticated for mass rearing to provide sufficiently large numbers of individuals for releases. Increases in productivity of domesticated tephritid strains are well documented, but there have been few systematic studies of the genetic consequences of domestication in tephritids. Here, we used nine DNA microsatellite markers to monitor changes in genetic diversity during the early generations of domestication in replicated lines of the fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). The observed changes in heterozygosity and allelic richness were compared with the expected changes in heterozygosity generated by a stochastic simulation including genetic drift but not selection. The results showed that repeatable genetic bottlenecks occur in the early generations and that selection occurs in the later generations. Furthermore, using the same simulation, we show that there is inadvertent selection for increased productivity for the entire life on a mass-rearing colony, in addition to intentional selection for increased productivity. That additional selection results from the common practice of establishing the next generation of the breeding colony from a small proportion of one day's pupae collection (the pupal raffle). That selection occurs during all generations and acts only on fecundity variation. Practical methods to counter that unavoidable loss of genetic diversity during the domestication process in B. tryoni are discussed.     

Volatile host fruit odors as attractants for the oriental fruit fly (Diptera: Tephritidae)

We examined the responses of oriental fruit flies, Bactrocera dorsalis Hendel, to the odors of different stages and types of fruit presented on potted trees in a field cage. Females were most attracted to odors of soft, ripe fruit. Odors of common guava were more attractive to females than papaya and starfruit, and equally as attractive as strawberry guava, orange, and mango. In field tests, McPhail traps baited with mango, common guava, and orange captured equal numbers of females. Traps baited with mango were compared with 2 commercially available fruit fly traps. McPhail traps baited with mango captured more females than visual fruit-mimicking sticky traps (Ladd traps) and equal numbers of females as McPhail traps baited with protein odors. Results from this study indicate that host fruit volatiles could be used as lures for capturing oriental fruit flies in orchards.