GENETIC DIVERGENCE ALONG THE SPECIATION CONTINUUM: THE TRANSITION FROM HOST RACE TO SPECIES IN RHAGOLETIS (DIPTERA: TEPHRITIDAE)

Studies of related populations varying in their degrees of reproductive isolation can provide insights into speciation. Here, the transition from partially isolated host races to more fully separated sibling species is investigated by comparing patterns of genetic differentiation between recently evolved (～150 generations) apple and ancestral hawthorn‐infesting populations of Rhagoletis pomonella to their sister taxon, the undescribed flowering dogwood fly attacking Cornus florida. No fixed or diagnostic private alleles differentiating the three populations were found at any of 23 microsatellites and 10 allozymes scored. Nevertheless, allele frequency differences were sufficient across loci for flowering dogwood fly populations from multiple localities to form a diagnosable genotypic cluster distinct from apple and hawthorn flies, indicative of species status. Genome‐wide patterns of differentiation were correlated between the host races and species pair comparisons along the majority of chromosomes, suggesting that similar disruptive selection pressures affect most loci. However, differentiation was more pronounced, with some additional regions showing elevated divergence, for the species pair comparison. Our results imply that Rhagoletis sibling species such as the flowering dogwood fly represent host races writ large, with the transition to species status primarily resulting from increased divergence of the same regions separating apple and hawthorn flies.     

Experimental evidence of genome‐wide impact of ecological selection during early stages of speciation‐with‐gene‐flow

Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.     

REGIONAL,LOCAL AND MICROGEOGRAPHIC ALLELE FREQUENCY VARIATION BETWEEN APPLE AND HAWTHORN POPULATIONS OF RHAGOLETIS POMONELLA IN WESTERN MICHIGAN

In the preceding study (Feder et al., 1990), we report that paired apple and hawthorn infesting populations of Rhagoletis pomonella are genetically differentiated for six allozymes. Here, we show that patterns of intra- and inter-host allele frequency variation seen for these six loci across the eastern United States are consistent on a more fine grained spatial scale in western Michigan. Malic enzyme, Aconitase-2, Mannose phosphate isomerase, and Hydroxyacid dehydrogenase all displayed significant linear relationships with latitude among five “regional” hawthorn populations sampled along a north-south transect between the cities of Cadillac and Portage, Michigan. Clines were not as evident among “regional” apple populations in western Michigan, although allele frequencies for Malic enzyme¹⁰⁰, Mannose phosphate isomerase¹⁰⁰ and Aconitase-2⁹⁵ varied with latitude among six “local” apple populations within a 60 km² area near the town of Grant. Significant allele frequency differences were observed between hawthorn and apple populations at all “regional” and “local” collecting sites analyzed in the study (a total of 20 different apple and hawthorn populations). As was the case in the geographic survey of the eastern United States, the magnitude and pattern of inter-host frequency differences at “regional” and “local” sites were a function of latitude. Host related genetic differentiation was consistent on a “microgeographic” scale as well. Allele frequencies for Malic enzyme¹⁰⁰ and Aconitase-2⁹⁵ were significantly higher over a four-year period (1984 to 1987) for flies sampled from individual hawthorn trees (N = 6) than apple trees (N = 7) within an old field (0.09-km² area) located near Grant. The fine level of genetic subdivision between hawthorn and apple populations of R. pomonella in western Michigan substantiates the existence of host associated polymorphism in the fly and supports a sympatric mode of divergence for the “apple race”.     

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.     

The effects of climate, host plant phenology and host fidelity on the genetics of apple and hawthorn infesting races ofRhagoletis pomonella

True fruit flies belonging to theRhagoletis pomonella (Walsh) sibling species complex have been proposed to speciate sympatrically by shifting and adapting to new host plants. Here, we report the results from a series of ecological and genetic experiments conducted at a study site near Grant, Michigan, U.S.A., aimed at clarifying the relationship between host specialization and reproductive isolation for these flies. Our findings indicate that apple (Malus pumila) and hawthorn (Crataegus mollis) infesting populations ofR. pomonella are partially allochronically isolated. Differences in the timing of adult eclosion account for part of the allochronic divergence, as apple adults emerge approximately ten days earlier than hawthorn flies in the field. Genetic analyses across different life history stages of the fly show that adults do not randomly move between apple and hawthorn trees, but trend to attack the same species of plant that they infested as larvae. Estimates of interhost migration from the allozyme data suggest that from 2.8 to 10% of the apple population is of hawthorn origin and that over 20% of the hawthorn population is of apple origin. The length and quality of the growing season appear to affect the genetic composition of the host races, as allele frequencies in the hawthorn population are correlated with ambient temperature and rainfall during the spring of the preceding year. Finally, allele frequencies for six allozyme loci displaying host associated differentiation also show significant linear regressions with the timing of adult eclosion within both races. These regressions establish a link between allozyme loci displaying inter-host differentiation and a developmental trait (adult eclosion) responsible for partially isolating the races. The slopes of the regressions are paradoxical, however, as they suggest that apple adults should eclose later, not earlier, than hawthorn flies. We conclude by discussing potential resolutions to the eclosion time paradox.     

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.     

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 role of sexual isolation during rapid ecological divergence: Evidence for a new dimension of isolation in Rhagoletis pomonella

The pace of divergence and likelihood of speciation often depends on how and when different types of reproductive barriers evolve. Questions remain about how reproductive isolation evolves after initial divergence. We tested for the presence of sexual isolation (reduced mating between populations due to divergent mating preferences and traits) in Rhagoletis pomonella flies, a model system for incipient ecological speciation. We measured the strength of sexual isolation between two very recently diverged (~170 generations) sympatric populations, adapted to different host fruits (hawthorn and apple). We found that flies from both populations were more likely to mate within than between populations. Thus, sexual isolation may play an important role in reducing gene flow allowed by early-acting ecological barriers. We also tested how warmer temperatures predicted under climate change could alter sexual isolation and found that sexual isolation was markedly asymmetric under warmer temperatures – apple males and hawthorn females mated randomly while apple females and hawthorn males mated more within populations than between. Our findings provide a window into the early speciation process and the role of sexual isolation after initial ecological divergence, in addition to examining how environmental conditions could shape the likelihood of further divergence.     

Rapid and repeatable host plant shifts drive reproductive isolation following a recent human-mediated introduction of the apple maggot fly,Rhagoletis pomonella

Ecological speciation via host-shifting is often invoked as a mechanism for insect diversification, but the relative importance of this process is poorly understood. The shift of Rhagoletis pomonella in the 1850s from the native downy hawthorn, Crataegus mollis, to introduced apple, Malus pumila, is a classic example of sympatric host race formation, a hypothesized early stage of ecological speciation. The accidental human-mediated introduction of R. pomonella into the Pacific Northwest (PNW) in the late 1970s allows us to investigate how novel ecological opportunities may trigger divergent adaptation and host race formation on a rapid timescale. Since the introduction, the fly has spread in the PNW, where in addition to apple, it now infests native black hawthorn, Crataegus douglasii, and introduced ornamental hawthorn, Crataegus monogyna. We use this “natural experiment” to test for genetic differentiation among apple, black, and ornamental hawthorn flies co-occurring at three sympatric sites. We report evidence that populations of all three host-associations are genetically differentiated at the local level, indicating that partial reproductive isolation has evolved in this novel habitat. Our results suggest that conditions suitable for initiating host-associated divergence may be common in nature, allowing for the rapid evolution of new host races when ecological opportunity arises.     

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.     

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.     

Standing geographic variation in eclosion time and the genomics of host race formation in Rhagoletis pomonella fruit flies

Taxa harboring high levels of standing variation may be more likely to adapt to rapid environmental shifts and experience ecological speciation. Here, we characterize geographic and host‐related differentiation for 10,241 single nucleotide polymorphisms in Rhagoletis pomonella fruit flies to infer whether standing genetic variation in adult eclosion time in the ancestral hawthorn (Crataegus spp.)‐infesting host race, as opposed to new mutations, contributed substantially to its recent shift to earlier fruiting apple (Malus domestica). Allele frequency differences associated with early vs. late eclosion time within each host race were significantly related to geographic genetic variation and host race differentiation across four sites, arrayed from north to south along a 430‐km transect, where the host races co‐occur in sympatry in the Midwest United States. Host fruiting phenology is clinal, with both apple and hawthorn trees fruiting earlier in the North and later in the South. Thus, we expected alleles associated with earlier eclosion to be at higher frequencies in northern populations. This pattern was observed in the hawthorn race across all four populations; however, allele frequency patterns in the apple race were more complex. Despite the generally earlier eclosion timing of apple flies and corresponding apple fruiting phenology, alleles on chromosomes 2 and 3 associated with earlier emergence were paradoxically at lower frequency in the apple than hawthorn host race across all four sympatric sites. However, loci on chromosome 1 did show higher frequencies of early eclosion‐associated alleles in the apple than hawthorn host race at the two southern sites, potentially accounting for their earlier eclosion phenotype. Thus, although extensive clinal genetic variation in the ancestral hawthorn race exists and contributed to the host shift to apple, further study is needed to resolve details of how this standing variation was selected to generate earlier eclosing apple fly populations in the North.     

The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles

The Rhagoletis species complex has been a key player in the sympatric speciation debate for much of the last 50 years. Studies indicate that differences in olfactory preference for host fruit volatiles could be important in reproductively isolating flies infesting each type of fruit via premating barriers to gene flow. Single sensillum electrophysiology was used to compare the response characteristics of olfactory receptor neurons from apple, hawthorn, and flowering dogwood-origin populations of R. pomonella, as well as from the blueberry maggot, R. mendax (an outgroup). Eleven volatiles were selected as stimuli from behavioral/electroantennographic studies of the three R. pomonella host populations. Previously, we reported that differences in preference for host fruit volatile blends are not a function of alterations in the general class of receptor neurons tuned to key host volatiles. In the present study, population comparisons involving dose–response trials with the key volatiles revealed significant variability in olfactory receptor neuron sensitivity and temporal firing pattern both within and among Rhagoletis populations. It is concluded that such variability in peripheral sensitivity and temporal firing pattern could influence host preference and contribute to host fidelity and sympatric host shifts in the Rhagoletis complex.     

Multiple Wolbachia infections in Rhagoletis pomonella

Rhagoletis pomonella Walsh (Diptera: Tephritidae) is a model species for sympatric speciation through host race formation on apple and hawthorn. The bacterial endosymbiont Wolbachia, a manipulator of arthropod reproduction, has been considered to contribute to speciation in several species. A potential role of Wolbachia in sympatric speciation of R. pomonella remains to be tested despite an earlier detection by PCR. In this study, we isolated Wolbachia from R. pomonella individuals from both host species using multi‐locus sequence typing (MLST) and the surface protein wsp. By cloning and sequencing of 311 plasmids, we found sequence types of at least four wPom strains. A complete MLST profile was obtained only for wPom1, whereas MLST loci of the other putative strains were difficult to assign because of multiple infections and low sample numbers. wPom1 occurs in both host races, whereas different sequence types were found at low frequencies only in apple‐infesting R. pomonella. This warrants further investigation as it cannot be excluded that Wolbachia plays a part in this model of sympatric speciation.     

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.     

Rapid and repeatable shifts in life‐history timing of Rhagoletis pomonella (Diptera: Tephritidae) following colonization of novel host plants in the Pacific Northwestern United States

Host shifts of phytophagous insect specialists to novel plants can result in divergent ecological adaptation, generating reproductive isolation and potentially new species. Rhagoletis pomonella fruit flies in eastern North America underwent a host shift ~160 ya from native downy hawthorn (Crataegus mollis) to introduced, domesticated apple (Malus domestica). Divergent selection on diapause phenology related to the earlier fruiting time of apples versus downy hawthorns resulted in partial allochronic reproductive isolation between the fly races. Here, we test for how rapid and repeatable shifts in life‐history timing are driving ecological divergence of R. pomonella in the Pacific Northwestern USA. The fly was introduced into the region via larval‐infested apples 40–65 ya and now attacks native black hawthorn (Crataegus douglasii) and introduced ornamental hawthorn (Crataegus monogyna), in addition to early‐ and late‐maturing apple varieties in the region. To investigate the life‐history timing hypothesis, we used a field‐based experiment to characterize the host‐associated eclosion and flight activity patterns of adults, and the feeding times of larvae at a field site in Vancouver, Washington. We also assessed the degree to which differences in host‐fruiting time generate allochronic isolation among apple‐, black hawthorn‐, and ornamental hawthorn‐associated fly populations. We conclude that host‐associated fly populations are temporally offset 24.4% to 92.6% in their seasonal distributions. Our results imply that R. pomonella possesses the capacity for rapid and repeatable shifts in diapause life history to match host‐fruiting phenology, which can generate ecologically based reproductive isolation, and potentially biodiversity in the process.     

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 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.     

Are the apple maggot,Rhagoletis pomonella,and blueberry maggot,R. mendax,distinct species? Implications for sympatric speciation

Rhagoletis pomonella (Walsh) and R. mendax (Curran) (Diptera: Tephritidae) are major economic pests of apple and blueberry fruits, respectively, in eastern North America. The taxonomic status of these flies as distinct species has been in dispute because of their close morphological similarity, broadly overlapping geographic distributions and inter-fertility in laboratory crosses. Starch gel electrophoresis of soluble proteins was performed to establish the extent of genetic differentiation and levels of gene flow between blueberry infesting populations of R. mendax and apple and hawthorn infesting populations of R. pomonella. R. mendax and R. pomonella were found to be genetically distinct sibling species as eleven out of total of twenty-nine allozymes surveyed possessed species specific alleles. Data from three sympatric apple and blueberry fly populations in Michigan indicated that these flies do not hybridize in nature and gave no evidence for nuclear gene introgression. Differences in host plant recognition were implicated as important pre-mating barriers to gene flow between R. pomonella and R. mendax; a result supporting a sympatric mode of divergence for these flies.

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Résumé R. pomonella Walsh and R. mendax Curran sont respectivement deux mouches très nuisibles aux pommes et aux myrtilles du N E des USA. La position taxonomique de ces mouches comme espèces distinctes a été longtemps mise en doute par suite de leur grande ressemblance morphologique, de l'important chevauchement de leurs répartitions et de leur interfécondité au laboratoire. L'électophorèse sur gel d'amidon de protéines solubles a été utilisé pour établir l'importance de la différenciation génétique et du flux génique entre R. mendax contaminant des myrtilles et R. pomonella contaminant des pommiers et des aubépines. R. mendax et R. pomonella se sont révélées des espèces jumelles car, à l'exception de 11 alolozymes sur 29, chaque espèce possédait des allèles spécifiques. Les données concernant 3 populations sympatriques de mouches des myrtilles et des pommes du Michigan ont montré que des mouches ne s'hybrident pas dans la nature et n'ont fourni aucune indication sur une introgression de gènes nucléaires. Des différences concernant la découverte de hôtes sont impliquées comme obstacles prézygotiques importants au flux génique entre R. pomonella et R. mendax; ce résultat conforte l'hypothèse d'une divergence sympatrique de ces mouches.

     

Intra- and interspecific competition and host race formation in the apple maggot fly,Rhagoletis pomonella (Diptera: Tephritidae)

Intra- and interspecific resource competition are potentially important factors affecting host plant use by phytophagous insects. In particular, escape from competitors could mediate a successful host shift by compensating for decreased feeding performance on a new plant. Here, we examine the question of host plant-dependent competition for apple (Malus pumila)- and hawthorn (Crataegus mollis)-infesting larvae of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae) at a field site near Grant, Michigan, USA. Interspecific competition from tortricid (Cydia pomonella, Grapholita prunivora, and Grapholita packardi) and agonoxenid (subfamily Blastodacninae) caterpillars and a curculionid weevil (Conotrachelus crataegi) was much stronger for R. pomonella larvae infesting the ancestral host hawthorn than the derived host apple. Egg to pupal survivorship was estimated as 52.8% for fly larvae infesting hawthorn fruit without caterpillars and weevils compared to only 27.3% for larvae in harthorns with interspecific insects. Survivorship was essentially the same between fly larvae infesting apples in the presence (44.8%) or absence (42.6%) of interspecific insects. Intraspecific competition among maggots was also stronger in hawthorns than apples. The order or time that a larva exited a hawthorn fruit was a significant determinant of its pupal mass, with earlier emerging larvae being heavier than later emerging larvae. This was not the case for larvae in apples, as the order or time that a larva exited an apple fruit had relatively little influence on its pupal mass. Our findings suggest that decreased performance related to host plant chemistry/nutrition may restrict host range expansion and race formation in R. pomonella to those plants where biotic/ecological factors (i.e. escape from competitors and parasitoids) adequately balance the survivorship equation. This balance permits stable fly populations to persist on novel plants, setting the stage for the evolution of host specialization under certain mitigating conditions (e.g. when mating is host specific and host-associated fitness trade-offs exist).