The chemosensory basis for behavioral divergence involved in sympatric host shifts. I. Characterizing olfactory receptor neuron classes responding to key host volatiles

The recent shift of Rhagoletis pomonella from its native host hawthorn to introduced, domestic apple has been implicated as an example of sympatric speciation. Recent studies suggest that host volatile preference might play a fundamental role in host shifts and subsequent speciation in this group. Single sensillum electrophysiology was used to test a proposed hypothesis that differences in R. pomonella olfactory preference are due to changes in the number or odor specificity of olfactory receptor neurons. Individuals were analyzed from apple, hawthorn, and flowering dogwood-origin populations, as well as from the blueberry maggot, Rhagoletis mendax Curran (an outgroup). Eleven compounds were selected as biologically relevant stimuli from previous electroantennographic/behavioral studies of the three R. pomonella populations to host fruit volatiles. Cluster analysis of 99 neuron responses showed that cells from all tested populations could be grouped into the same five classes, ranging from those responding to one or two volatiles to those responding to several host volatiles. Topographical mapping also indicated that antennal neuron locations did not differ by class or fly taxa. Our results do not support the hypothesis that differences in host preference among Rhagoletis populations are a result of alterations in the number or class of receptor neurons responding to host volatiles.     

Comparing peripheral olfactory coding with host preference in the rhagoletis species complex

Recent studies have shown that flies from sympatric populationsof Rhagoletis pomonella infesting hawthorn, apple, and floweringdogwood fruit can distinguish among unique volatile blends identifiedfrom each host. Analysis of peripheral chemoreception in Rhagoletisflies suggests that changes in receptor specificity and/or receptorneuron sensitivity could impact olfactory preference among thehost populations and their hybrids. In an attempt to validatethese claims, we have combined flight tunnel analyses and singlesensillum electrophysiology in F₂ and backcross hybrids displayinga variety of behavioral phenotypes. Results show that differencesin peripheral chemoreception among second-generation adultsdo not provide a direct correlation between peripheral codingand olfactory behavior. We conclude that either the plasticityof the central nervous system in Rhagoletis can compensate forsignificant alterations in peripheral coding or that peripheralchanges present subtle effects on behavior not easily detectablewith current techniques. The results of this study imply thatthe basis for olfactory behavior in Rhagoletis has a complicatedgenetic and neuronal basis, even for populations with a recentdivergence in preference.     

Rhagoletis sibling species and host races differ in host odor recognition

Electronantennograms (EAG) were recorded from the apple and hawthorn host race of the apple maggot fly, Rhagoletis pomonella (Walsh), and from the blueberry maggot fly, R. mendax (Curran) (Diptera: Tephritidae), in response to host fruit extracts and nine volatile host fruit odor compounds at six concentrations. Mean relative EAG response to apple odor is the same in both species, but in respect to blueberry odor, it is significantly stronger in R. mendax than in both host races of R. pomonella (P<0.05), indicating that antennal sensitivity is selectively adapted to species specific host fruit odors. Differences in antennal response to several host fruit odor compounds were found between both species as well as between the host races. This indicates differences in antennal receptor cell types and/or numbers between species and host races. The flies had no prior host fruit experience which indicates that the measured differences are genetically based. Because Rhagoletis fruit flies are highly host specific parasites which meet and mate on their respective host plants, the results suggest that antennal sensitivity plays an important role in host shifts and speciation in this genus.

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Zusammenfassung Elektroantennogramme (EAG) der Apfel- und der Weissdorn-Wirtsrasse der Apfelfruchtfliege, Rhagoletis pomonella, und der Blaubeerenfruchtfliege, Rhagoletis mendax (Diptera: Tephritidae), wurden aufgezeichnet als Reizantworten auf Wirtsfruchtextrakte und auf neun flüchtige Duftkomponenten ihrer Wirtsfrüchte in sechs Konzentrationen. Die Sensitivität der Antennen bezüglich Apfelduft ist in beiden Arten gleich, aber die Reizantwort von R. mendax auf den Duft ihrer spezifischen Wirtsfrucht, Blaubeeren, ist signifikant stärker als diejenige beider Wirtsrassen von R. pomonella (P<0.05), was darauf hinweist, dass die antennale Sensitivität möglicherwiese an den artspezifischen Wirtsfruchtduft adaptiert ist. Unterschiede in der antennalen Reizantwort auf mehrere Duftkomponenten der Wirtsfrüchte konnten sowohl zwischen den Arten als auch Wirtsrassen gefunden werden. Dies deutet auf Unterschiede in antennalen Rezeptorzelltypen und/oder Rezeptorzellzahl zwischen Arten und Wirtsrassen. Die Unterschiede wurden von Individuen aufgezeichnet, die keine vorherige Erfahrung mit den Wirtsfrüchten hatten und sind daher genetischen Ursprungs. Fruchtfliegen der Gattung Rhagoletis sind stark wirtsspezifische Pflanzenparasiten, die ihre Wirtspflanze als Treffpunkt und Paarungsort benützen. Diese Resultate deuten daher darauf hin, dass antennale Sensitivität eine wichtige Rolle in Wirtswechseln und Speziation in diesem Genus spielt.

     

A second case of genetic host races in Rhagoletis? A population genetic comparison of sympatric host populations in the European cherry fruit fly,Rhagoletis cerasi

Despite an increasing acceptance in the biological community for sympatric speciation as a mode of species formation, well documented examples of sympatrically evolved ‘incipient species’ remain rare. The sympatric host races of apple maggot, Rhagoletis pomonella (Walsh), represent one of the most prominent case studies for sympatric speciation via a host shift. The European cherry fruit fly, R. cerasi (L.), shows strong ecological similarities to R. pomonella: (1) infestation of two different host plants, Lonicera xylosteum L. and Prunus avium L., and (2) divergent phenological and behavioral adaptations of flies on different hosts. The population genetic study presented here addresses whether the host associated populations of R. cerasi also represent genetically differentiated true host races. Out of a total of 29 allozyme loci examined, six were polymorphic and used to analyze six sympatric pairs of R. cerasi populations on Lonicera and Prunus from Switzerland and Germany. A direct comparison of allele frequencies between sympatric sites showed no pattern indicative of host races in R. cerasi. However, the hierarchical F‐statistic for one locus, mannose 6‐phosphate isomerase (Mpi), showed significant population differentiation that was in accordance with host race differentiation. Mpi is one of several loci that are also diagnostic for host race differentiation in R. pomonella. Results from Mpi suggest the formation of sympatric host races in R. cerasi, but additional polymorphic markers are necessary.     

Behavioral evidence for host races in Rhagoletis pomonella flies

Summary One of the most controversial putative cases of host race formation in insects is that of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). A principal cause of the controversy is lack of relevant data. In laboratory and field enclosure experiments, we compared the host acceptance behavior of sympatric populations of flies originating from naturally infested hawthorn (the native host) and apple (an introduced host) in Amherst, Massachusetts or East Lansing, Michigan. In general, hawthorn fruit were accepted for ovipositional attempts nearly equally by apple and hawthorn origin females, whereas apples were accepted much more often by apple than hawthorn origin females. Similarly, males of apple and hawthorn origin exhibited about equal duration of residence on hawthorn fruits as sites at which to acquire potential mates, while males of apple origin tended to reside substantially longer than males of hawthorn origin on apples. Irrespective of fly origin, both sexes always responded more positively to hawthorn fruit than to apples. Because all flies assayed were naive (ruling out effects of prior host experience of adults) and because tests revealed no influence of pre-imaginal fruit exposure on pattern of host fruit acceptance by females, the combined evidence suggests the phenotypic differences we observed in host response pattern between hawthorn and apple origin flies may have an underlying genetic basis. Further tests showed that while larval progeny of flies of each origin survived better in naturally growing hawthorn fruit than in naturally growing apples, there was no differential effect of fly origin on larval survival ability in either host. We discuss our findings in relation to restriction in gene flow between sympatric populations of R. pomonella and in relation to current models of host shifts in insects.     

Variability in response specificity of apple, hawthorn, and flowering dogwood-infesting Rhagoletis flies to host fruit volatile blends: implications for sympatric host shifts

Rhagoletis pomonella Walsh (Diptera: Tephritidae) originating from domesticated apple (Malus pumila), hawthorn (Crataegus mollis) (Rosaceae), and flowering dogwood (Cornus florida) (Cornaceae) were tested sequentially in flight‐tunnel assays to volatile blends previously identified from the three fruit types. The majority of flies flew to odor sources containing their natal blend (68–83%). Some flies from each fruit type also flew to non‐natal fruit blends (11–39%), but of these non‐natal responders the vast majority were flies that responded to their natal blend as well. The results indicate that individual flies within R. pomonella populations infesting different host types have different degrees of specificity with respect to discriminating among fruit volatile blends, and that a moderate proportion of apple, hawthorn, and dogwood flies (10–30%) are broad responders, with the capacity to recognize and orient to more than one blend. The observed variability in response specificity could facilitate sympatric shifts to new host plants.     

Geographic variation in fruit volatiles emitted by the hawthorn Crataegus mollis and its consequences for host race formation in the apple maggot fly,Rhagoletis pomonella

The shift of the apple (AP) maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), from its ancestral host downy hawthorn, Crataegus mollis (DH) (Torr. & A. Gray) Scheele, to introduced domesticated AP, Malus domestica Borkh. (both Rosaceae), is a model for ecological divergence and incipient sympatric speciation with gene flow. However, a portion of the variation contributing to the sympatric host shift from DH to AP appears to have a different biogeographic history, pre‐dating the shift. One potential source of standing variation may trace to a number of different native hawthorn species infested by R. pomonella in the southern USA, where the AP‐attacking race is absent. Herein, we investigate this possibility for the southern red hawthorn (SR) endemic to Texas, Crataegus mollis var. texana (Buckl.), which has been described as a member of the Molles series that includes the more northern distributed DH. We report results from chemical analyses of host fruit volatiles, fly behavioural responses to synthetic fruit blends, and microsatellite surveys of fly populations, implying that R. pomonella infesting SR may behaviourally and genetically represent a native host race differing from the DH‐infesting fly. No fly reared from SR responded to AP fruit volatiles in flight tunnel assays. However, coupled gas chromatographic‐electroantennographic detection (GC‐EAD) profiles for SR fruit contain all five of the component esters that comprise the standard AP volatile blend inducing behavioural orientation for AP‐infesting flies, compounds that appear to be largely missing from volatile profiles for DH fruit. Thus, SR‐infesting flies do not represent a source for a preassembled AP‐accepting phenotype. However, they may help explain why the ancestral DH race that shifted to AP in the northeastern USA had the ability to recognize AP fruit esters, potentially enabling the shift to AP. Our results highlight how categorizing speciation into different geographic modes may not adequately describe the evolutionary origins of important genetic variation fuelling adaptive radiation and the genesis of new biodiversity.     

Antagonist effects of non-host fruit volatiles on discrimination of host fruit by Rhagoletis flies infesting apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida)

In previous flight‐tunnel tests Rhagoletis pomonella (Walsh) (Diptera: Tephritidae) flies originating from domestic apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida), displayed greater numbers of upwind flights to blends of volatiles identified from their natal fruit compared to non‐natal fruit. Here, we show that when certain non‐host volatiles were added to the host blend, significantly fewer apple, hawthorn, and dogwood flies exhibited sustained upwind flight to the source. Specifically, the upwind flight of apple flies to the apple blend was significantly antagonized by the addition of the hawthorn or dogwood blends, the addition of 3‐methylbutan‐1‐ol alone (a key volatile for hawthorn and dogwood flies), or the combination of 3‐methylbutan‐1‐ol and another key dogwood volatile, 1‐octen‐3‐ol. Similarly, the upwind flight of dogwood and hawthorn flies to their respective natal blends was antagonized by the addition of the apple blend or the key apple volatile butyl hexanoate. Experiments were also conducted to determine whether non‐natal fruit volatiles could disrupt the close‐range flight response of flies to the visual stimulus of fruit alone, represented by an odorless red sphere. Tests with apple‐origin flies showed that when the hawthorn blend, the dogwood blend, or the key antagonist volatiles from each (3‐methylbutan‐1‐ol and 1‐octen‐3‐ol) were added to a red sphere fruit mimic, significantly lower proportions of flies were captured, compared with captures when no odor was present. Our results support the hypothesis that agonist and antagonist properties of fruit volatiles can play an important role in host recognition/discrimination by Rhagoletis flies.     

The diapause response of Rhagoletis pomonella to varying environmental conditions and its significance for geographic and host plant‐related adaptation

The recent shift of Rhagoletis pomonella Walsh (Diptera: Tephritidae) from its ancestral host hawthorn to apple is a model for incipient sympatric speciation in action. Previous studies have shown that changes in the over‐wintering pupal diapause are critical for differentially adapting R. pomonella flies to a difference in the fruiting times of apples vs. hawthorns, generating ecologically based reproductive isolation. Here, we exposed pupae of the hawthorn race to various combinations of pre‐ and over‐wintering rearing conditions and analyzed their effects on eclosion time and genetics. We report certain unexpected results in regards to a combination of brief pre‐winter and over‐wintering periods indicative of gene*environment interactions requiring a reassessment of our current understanding of R. pomonella diapause. We present a hypothesis that involves physiological factors related to stored energy reserves in pupae that influences the depth and duration of Rhagoletis diapause. This ‘pupal energy reserve’ hypothesis can account for our findings and help clarify the role host plant‐related life history adaptation plays in phytophage biodiversity.     

Genetic variation among apple and hawthorn host races of Rhagoletis pomonella across an ecological transition zone in the Mid-Western United States

In previous studies, we have shown that apple and hawthorn populations of Rhagoletis pomonella (Diptera: Tephritidae) represent partially reproductively isolated and genetically differentiated host races; a result consistent with predictions of sympatric speciation models. The geographic pattern of allozyme variation for these flies is complex, however, as inter-host differences are superimposed on latitudinal allele frequency clines within the races. In addition, pronounced allele frequency shifts exist among R. pomonella populations across three major ecological transition zones in the mid-western United States. This suggests that selection related to environmental heterogeneity is responsible for the allele frequency shifts, but does not rule out secondary contact as an alternative possibility. Resolution of this issue is important, because if secondary contact is involved, then we would have to reassess the relationship host race formation has with speciation in the R. pomonella group.Here, we present results from a detailed genetic analysis of fly populations spanning the deciduous/prairie transition zone near the border between the states of Wisconsin and Illinois. Allele frequencies for hawthorn populations within the zone formed spikes, rather than the expected steps, and these frequency peaks correlated with variation in local ambient temperature conditions. Ambient temperature, and not secondary contact, therefore appears to be an important determinant of the shape of R. pomonella allele frequency clines. Allele frequency heterogeneity was also observed among apple populations, but was less pronounced compared to that for hawthorn flies. This suggests that ambient temperature differentially affects the host races, possibly through differences in the fruiting phenologies of apple and hawthorn trees. Several pairs of linked loci displayed concordant allele frequency changes and were in disequilibrium among both apple and hawthorn populations along the Wisconsin/Illinois transect. Although we do not know the reason for the observed pattern of disequilibrium, site to site variation in levels of inter-host migration, coupled with selection, seem the most likely explanations. We conclude by discussing how host specific adaptations, such as those associated with ambient temperature, may interact with host recognition traits to drive the sympatric speciation process for R. pomonella group flies.     

Evidence for sexual isolation as a prezygotic barrier to gene flow between morphologically divergent species of Rhagoletis fruit flies

1. Certain groups of fruit flies in the genus Rhagoletis (Diptera: Tephritidae) are exemplars for sympatric speciation via host plant shifting. Flies in these species groups are morphologically similar and overlap in their geographic ranges, yet attack different, non‐overlapping sets of host plants. Ecological adaptations related to differences in host choice and preference have been shown to be important prezygotic barriers to gene flow between these taxa, as Rhagoletis flies mate on or near the fruit of their respective host plants. Non‐host‐related assortative mating is generally absent or present at low levels between these sympatrically diverging fly populations. 2. However, some Rhagoletis taxa occasionally migrate to ‘non‐natal’ plants that are the primary hosts of other, morphologically differentiated fly species in the genus. These observations raise the question of whether sexual isolation may reduce courtship and copulation between morphologically divergent species of Rhagoletis flies, contributing to their prezygotic isolation along with host‐specific mating. 3. Using reciprocal multiple‐choice mating trials, we measured sexual isolation among nine species pairs of morphologically differentiated Rhagoletis flies. Complete sexual isolation was observed in eight of the nine comparisons, while partial sexual isolation was observed in the remaining comparison. 4. We conclude that sexual isolation can be an effective prezygotic barrier to gene flow contributing to substantial reproductive isolation between many morphologically distinct Rhagoletis species, even in the absence of differential host plant choice and host‐associated mating.     

Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella

Ecological speciation with gene flow may be an important mode of diversification for phytophagous insects. The recent shift of Rhagoletis pomonella from its native host downy hawthorn (Crataegus mollis) to introduced apple (Malus domestica) in the northeastern United States is a classic example of sympatric host race formation. Here, we test whether R. pomonella has similarly formed host races on four native Crataegus species in the southern United States: western mayhaw (C. opaca), blueberry hawthorn (C. brachyacantha), southern red hawthorn (C. mollis var. texana) and green hawthorn (C. viridis). These four southern hosts differ from each other in their fruiting phenology and in the volatile compounds emitted from the surface of their fruits. These two traits form the basis of ecological reproductive isolation between downy hawthorn and apple flies in the north. We report evidence from microsatellite population surveys and eclosion studies supporting the existence of genetically differentiated and partially reproductively isolated host races of southern hawthorn flies. The results provide an example of host shifting and ecological divergence involving native plants and imply that speciation with gene flow may be commonly initiated in Rhagoletis when ecological opportunity presents itself.     

BEHAVIORAL EVIDENCE FOR FRUIT ODOR DISCRIMINATION AND SYMPATRIC HOST RACES OF RHAGOLETIS POMONELLA FLIES IN THE WESTERN UNITED STATES

The recent shift of Rhagoletis pomonella (Diptera: Tephritidae) from its native host downy hawthorn, Crataegus mollis, to introduced domesticated apple, Malus domestica, in the eastern United States is a model for sympatric host race formation. However, the fly is also present in the western United States, where it may have been introduced via infested apples within the last 60 years. In addition to apple, R. pomonella also infests two hawthorns in the West, one the native black hawthorn, C. douglasii, and the other the introduced English ornamental hawthorn, C. monogyna. Here, we test for behavioral evidence of host races in the western United States. through flight tunnel assays of western R. pomonella flies to host fruit volatile blends. We report that western apple, black hawthorn, and ornamental hawthorn flies showed significantly increased levels of upwind‐directed flight to their respective natal compared to nonnatal fruit volatile blends, consistent with host race status. We discuss the implications of the behavioral results for the origin(s) of western R. pomonella, including the possibility that western apple flies were not introduced, but may represent a recent shift from local hawthorn fly populations.     

THE GEOGRAPHIC PATTERN OF GENETIC DIFFERENTIATION BETWEEN HOST ASSOCIATED POPULATIONS OF RHAGOLETIS POMONELLA (DIPTERA: TEPHRITIDAE) IN THE EASTERN UNITED STATES AND CANADA

True fruit flies in the Rhagoletis pomonella sibling species group are at the center of a long-standing debate concerning modes of speciation. The allopatric separation of populations is widely thought to be a prerequisite for speciation in sexually reproducing animals. However, speciation in the R. pomonella group appears to have occurred sympatrically as a consequence of these flies shifting and adapting to new host plants. The sympatric shift of R. pomonella from its native host hawthorn to introduced domestic apple, which occurred approximately 150 years ago, provides a test of whether host specialization is sufficient to allow populations to differentiate in the absence of geographic barriers to gene flow. We report the results of a geographic study of allozyme variation for hawthorn and apple infesting populations of R. pomonella across the eastern United States and Canada. Six loci consistently show significant allele frequency differences at paired apple and hawthorn sites. These six loci map to three different regions of the genome, and linkage disequilibrium exists between non-allelic genes within each of these regions. Allele frequencies for five of the six loci displaying host associated differences also co-vary significantly with latitude. Inter-host divergence is, therefore, superimposed on north-south clinal patterns of intra-host variation such that the magnitude of genetic divergence between hawthorn and apple flies is a function of latitude. The findings suggest that partially reproductively isolated “host races” can evolve in sympatry as a consequence of R. pomonella infesting new host plants. Host recognition and host associated developmental traits are discussed as important factors differentiating apple and hawthorn flies.     

On the scent of standing variation for speciation: behavioral evidence for native sympatric host races of rhagoletis pomonella (Diptera: tephritidae) in the southern United States

Standing variation can be critical for speciation. Here, we investigate the origins of fruit odor discrimination for Rhagoletis pomonella underlying the fly's sympatric shift in the northeastern United States from downy hawthorn (Crataegus mollis) to apple (Malus domestica). Because R. pomonella mate on host fruit, preferences for natal fruit volatiles generate prezygotic isolation. Apples emit volatiles that appear to be missing from gas chromatography/electroantennographic detection profiles for flies infesting downy hawthorns, raising the question of how R. pomonella evolved a preference for apple. In the southern United States, R. pomonella attacks several native hawthorns. Behaviorally active volatile blends for R. pomonella infesting southern hawthorns contain the missing apple volatiles, potentially explaining why downy hawthorn flies could have evolved to be sensitive to a blend of apple volatiles. Flight tunnel assays imply that southern hawthorn populations were not the antecedent of a preassembled apple race, as southern flies were not attracted to the apple volatile blend. Instead, behavioral evidence was found for southern host races on native hawthorns, complementing the story of the historical sympatric shift to introduced apple in the North and illustrating how R. pomonella may evolve novel combinations of agonist and antagonist responses to volatiles to use new fruit resources.     

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.     

Host fruit chemical stimuli eliciting distinct ovipositional responses from sibling species of Rhagoletis fruit flies

Laboratory experiments tested whether two economically-important sibling species of tephritid fruit flies have evolved distinct egg-laying responses to chemical stimuli on the fruits of their respective hostplants. The egg-laying preferences displayed by apple maggot flies, R. pomonella, and blueberry maggot flies, R. mendax, on artificial fruits treated with apple and blueberry extract paralleled their egg-laying responses to whole apples and blueberries. R. pomonella flies laid more eggs than R. mendax flies in artificial fruits treated with extract from ripe McIntosh apples, and vice versa for artificial fruits treated with extract from ripe Bluehaven blueberries. Furthermore, both species laid more eggs in artificial fruits treated with extract from their respective host fruits than control artificial fruits which were not treated with fruit extract. Prior electroantennogram recordings from R. mendax and R. pomonella flies exposed to volatiles from pentane extracts of apples and blueberries indicate that the antennal sensitivity of both species is selectively tuned to their respective host fruit odors. This differentiation in their olfactory responses to fruit odors could be important in mediating their distinct ovipositional responses to blueberry and apple fruits. Extract from unripe McIntosh apples also elicited egg laying by R. pomonella flies, however, artificial fruits treated with unripe apple extract received 1.9 times fewer eggs than those treated with ripe apple extract. Moreover, the numbers of R. pomonella ovipositor punctures and eggs placed in wax artificial fruits were increased when the artificial fruits were treated with a blend of 7 identified apple esters. Black coloration on these artificial fruits and the presence of apple esters had a synergistic effect on the egg-laying behavior of R. pomonella flies, which caused them to lay substantially more eggs per black fruit than white fruit treated with the same concentration of apple esters. In summary, our results indicate that the egg-laying responses of R. pomonella flies are mediated by the integration of information from fruit chemical and visual cues, and that R. mendax and R. pomonella flies have evolved divergent egg-laying responses to chemical stimuli on the fruits of their respective hostplants. These findings are discussed in the context of other studies on plant compounds which influence the ovipositional behavior of phytophagous Diptera.

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Stimuli chimiques des pommes et des myrtilles induisant la ponte des espèces jumelles, Rhagoletis pomonella et R. mendax

Résumé Des fruits artificiels en cire traités avec des extraits de fruits ont provoqué chez les espèces jumelles de R. mendax (Curran) et R. pomonella (Walsh) des réactions de ponte différentes suivant les stimulations chimiques par les fruits. Le comportement de ponte sur des fruits artificiels traités avec des extraits au pentane des myrtilles mûres (Vaccinium corymbosum L.) et de pommes mûres (Malus pumila Miller = Pyrus malus L.), est le même que sur des fruits naturels, ce qui montre que la réponse aux stimulations chimiques provenant du fruit constitue un aspect important de la reconnaissance de l'hôte. R. pomonella pond plus d'ufs que R. mendax sur les fruits artificiels traités à l'extrait de pommes mûres; c'est l'inverse pour les fruits traités aux extraits de myrtille. Les fruits artificiels traités avec des pommes ou des myrtilles provoquent la ponte de R. pomonella, tandis que les myrtilles mûres seules provoquent la ponte de R. mendax. Les extraits de pommes vertes stimulent la ponte de R. pomonella mais elle est alors 2 fois plus faible qu'avec des extraits de pommes mûres. Un mélange de 7 esters identifiés dans l'extrait de pomme induit aussi la ponte de R. pomonella. Le nombre de piqûres de tarièresfli dans les fruits artificiels en cire et le nombre d'ufs par fruit ont été augmentés par addition d'esters de pommes à des fruits blancs ou noirs. La couleur des fruits artificiels influence aussi la réaction de ponte de R. pomonella; la fréquence des piqûres de tarière contenant un uf et le nombre d'ufs par fruit étaient significativement plus élevés sur les fruits noirs que sur les fruits blancs traités avec la même concentration d'esters de pomme. Les fruits artificiels noirs traités avec la concentration la plus stimulante d'esters de pommes ont reçu 2, 3 fois plus d'ufs que les fruits blancs avec les mêmes concentrations en esters. Ces résultats montrent que les esters de pomme et la couleur noire stimulent synergiquement la ponte de R. pomonella sur des fruits artificiels.

     

Divergence and evolution of reproductive barriers among three allopatric populations of Rhagoletis cingulata across eastern North America and Mexico

Geography is often a key factor facilitating population divergence and speciation. In this regard, the geographic distributions of flies in the genus Rhagoletis (Diptera: Tephritidae) in temperate North America have been affected by cycles of Pleistocene glaciation and interglacial periods. Fluctuations in climatic conditions may have had their most dramatic effects on geographically isolating Rhagoletis flies in the central highland region of Mexico. During past periods of allopatry, a degree of post‐zygotic reproductive isolation appears to have evolved between hawthorn‐infesting populations of Rhagoletis pomonella (Walsh) in the central Eje Volcanico Trans Mexicano (EVTM) and those from the Sierra Madre Oriental Mountains (SMO) of Mexico, as well as hawthorn flies from the eastern USA. Here, we investigate the generality of this finding in the genus Rhagoletis by testing for reproductive isolation among populations of Rhagoletis cingulata (Loew) (Diptera: Tephritidae) collected from infested domesticated sweet cherry (Prunus avium L.) in the USA and black cherry [Prunus serotina Ehrh. (both Rosaceae)] from the SMO and EVTM. We report evidence for marked post‐mating reproductive isolation among certain R. cingulata populations. The high levels of reproductive isolation were observed between R. cingulata flies from populations in the USA and SMO differed from the pattern seen for R. pomonella, primarily involving the EVTM. In addition, egg hatch was significantly reduced for crosses between SMO males and EVTM females, but not greatly in the opposite direction. We discuss potential causes for the different patterns of post‐mating reproductive isolation among Rhagoletis flies.     

The effect of prior adult experience on components of habitat preference in the apple maggot fly (Rhagoletis pomonella)

Summary Numerous authors have suggested that genetic subdivision within a population in a heterogeneous environment is more likely if individuals tend, through prior experience, to breed in the same habitat in which they developed. Under semi-field conditions we demonstrate that prior adult experience alters habitat preference in the apple maggot fly, Rhagoletis pomonella (Tephritidae), a frugivorous parasitic insect thought to have undergone sympatric divergence in host use in historical times. Females exposed to a particular host fruit species — apple (Malus pumila) or hawthorn (Crataegus mollis) — in a field cage oviposited at a higher rate in test fruit of that species than did inexperienced females or females exposed to the other species. Females exposed to a particular host fruit species also tended to remain longer in test trees harboring fruit of that species than did inexperienced females or females exposed to the other species. Prior adult experience thus alters two components of habitat preference in the apple maggot fly: oviposition preference and habitat fidelity. We discuss how these effects of experience on habitat preference should increase the likelihood that individuals mate assortatively and may further increase the likelihood that apple maggot populations become genetically subdivided.