ONE HOST SHIFT LEADS TO ANOTHER? EVIDENCE OF HOST‐RACE FORMATION IN A PREDACEOUS GALL‐BORING BEETLE

Abstract.— We show that a predator, the tumbling flower beetle Mordellistena convicta (Coleoptera: Mordellidae), has formed host races in response to a host-plant shift and subsequent host-race formation by its prey, the gall-inducing fly Eurosta solidaginis (Diptera: Tephritidae). This fly has formed two host races, one that induces stem galls on the ancestral host plant, Solidago altissima (Compositae), and another that induces stem galls on the closely related S. gigantea . We found that subpopulations of M. convicta that attack E. solidaginis galls on the different host plants have significantly different emergence times and, although slight, these allochronic differences are consistent across a range of temperatures. More importantly, we found that beetles assortatively mate according to their natal host plants, and female M. convicta preferentially attack and/or their offspring have higher survival in galls on natal host plants. Our data suggest that subpopulations of M. convicta that attack E. solidaginis galls on S. altissima and S. gigantea have formed host races. This is one of the first studies to demonstrate that a host shift and subsequent host-race formation by an herbivorous insect may have resulted in subsequent diversification by one of its natural enemies.     

Gall Flies, Inquilines, and Goldenrods: A Model for Host-race Formation and Sympatric Speciation

Host shifts and subsequent host-race formation likely play amore common role in the speciation of herbivorous insects thanhas generally been recognized. Our studies of the interactionsof goldenrod host plants (Solidago: Compositae), the gall flyEurosta solidaginis (Diptera: Tephritidae), and the stem- andgall-boring Mordellistena convicta (Coleoptera: Mordellidae)provide behavioral, ecological, and genetic evidence of insecthost races that may represent incipient species formed via sympatricspeciation. Eurosta solidaginis has developed genetically differentiatedand reproductively isolated host races that are associated withthe ancestral host Solidago altissima and the derived host S.gigantea. Conventional wisdom suggests that shifts even to closelyrelated host plants are limited by host preferences or the inabilityto utilize a chemically and developmentally distinct host. However,our preliminary work with Eurosta from S. gigantea implies thathost choice and gall induction do not deter a shift to S. canadensis.The galling of Solidago by Eurosta created a new resource thathas led to a subsequent host range expansion by the stem-boringbeetle. Mordellistena convicta from stems and galls are geneticallydistinct and likely shifted from stems to galls. Beetles fromS. altissima versus S. gigantea galls exhibit assortative matingand higher preference for and/or performance on their natalhost. The present-day distributions of the Eurosta host racesand their behavioral isolating mechanisms do not suggest thatgeographic isolation was required for their formation; ratherthese characteristics suggest a sympatric mode of differentiation.Our findings lend credence to recent assertions that sympatricspeciation may be an important source of biodiversity.     

BEHAVIORAL EVIDENCE FOR HOST-RACE FORMATION IN EUROSTA SOLIDAGINIS

We report behavioral evidence that Eurosta solidaginis, a stem-galling tephritid fly, has formed host races on its two goldenrod hosts, Solidago altissima and S. gigantea. Previous work has shown that flies from each host plant differ electrophoretically at the level of host races. The two host-associated populations were truly sympatric and were frequently found on host plants of the two species growing interdigitated with each other. Each host-associated population demonstrated a strong preference for ovipuncturing its own host. The S. gigantea–associated population emerged 10 to 14 d earlier than the S. altissima–associated population, contributing to the reproductive isolation between populations. Partial reproductive isolation is also maintained by a preference for mating on the host from which the fly emerged. The populations meet the criteria established for host races, suggesting that they may be in an intermediate stage of sympatric speciation.     

HYBRIDIZATION STUDIES ON THE HOST RACES OF EUROSTA SOLIDAGINIS: IMPLICATIONS FOR SYMPATRIC SPECIATION

We studied the inheritance of survival ability in host-associated populations of the tephritid fly, Eurosta solidaginis, to test predictions of sympatric speciation models. Eurosta solidaginis induces galls on two species of goldenrod, Solidago altissima and S. gigantea. The host-associated populations have been hypothesized to be host races that originated in sympatry (Craig et al. 1993). We found evidence for disruptive selection for host use, which is a critical assumption of sympatric speciation models. Each host race had higher survival rates on their host plant than on the alternative host. F₁ and backcross hybrids also had lower survival rates than the pure host-race flies on their host plant. Since assortative mating occurs due to host-plant preference (Craig et al. 1993) this would select for divergence in host preference. Low hybrid survival could have been due to strong genetic incompatibilities of the populations or due to host adaptation by each population. Strong genetic incompatibilities would result in poor survival on all host plants, while host adaptation could result in low overall survival with high hybrid survival on some host plants with particularly “benign” environments. High survival of F₁, F₂, and backcross hybrids on some plant genotypes in some years supported the host adaptation hypothesis. F₁ flies mated and oviposited normally and produced viable F₂ and backcross hybrids indicating gene flow is possible between the host races. A few flies developed and emerged on the alternative host plant. This demonstrates that genes necessary to utilize the alternative host exist in both host races. This could have facilitated the origin of one of the populations via a host shift from the ancestral host. The inheritance of survival ability appears to be an autosomal trait. We did not find evidence that survival ability was maternally influenced or sex linked.     

Cryptic speciation and host-race formation in a purportedly generalist tumbling flower beetle

Host-race formation remains controversial as a source of herbivorous insect diversity, and examples of host races are still fairly scarce. In this study, analysis of five enzyme loci in the ostensibly generalist tumbling flower beetle Mordellistena convicta (Coleoptera: Mordellidae) revealed hidden host-plant and plant-organ related genetic differentiation. Mordellistena convicta turned out to be a complex of cryptomorphic species, each with fewer hosts than the nominal species. These cryptic species, in turn, were divided into taxa that showed host-race characteristics: samples from different host plants and organs exhibited (1) genetic indications of partial reproductive isolation, (2) differences in size and emergence timing that suggested divergent host-related selection, and (3) among-host selective differences in mortality from parasitoids. Host-race formation in M. convicta, which has a somewhat different life history from the well-studied host races, enlarges the group of insects considered likely to undergo this process. The widespread sympatry of the M. convicta species complex, along with its spectrum of host-correlated genetic differentiation, suggests that these host specialist taxa developed in sympatry.     

Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation

Host-associated mating is crucial in maintaining the partial reproductive isolation between the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and S. gigantea. (We refer to flies reared from S. gigantea as gigantea flies and those reared from S. altissima as altissima flies.) We measured the host preference of males and females of both host races, F1 hybrids between the host races, F2, and backcrosses to both host races. Male and female altissima flies and female gigantea flies had high host fidelity, whereas male gigantea flies had low host fidelity. This result suggests that there may be gene flow between the host races due to nonassortative mating that occurs when male gigantea mate with altissima females on S. altissima. This indicates assortative-mating mechanisms in addition to host-associated mating are required to produce the partial reproductive isolation between the host races that has been observed. Nongenetic factors had no influence on host preference. Larval conditioning did not influence host preference: reciprocal F1 hybrids reared in S. altissima and S. gigantea both preferred S. gigantea. Adult experience had no impact on host preference: females preferred their natal host plant regardless of which host they encountered first as an adult. The hypothesis that maternal effects influence preferences was rejected because male and female flies did not show a consistent preference for the host plant of their mother. We also found no evidence that preference was a sex-linked trait because F1 and backcrosses to the host races with different combinations of X chromosomes from the two host races preferred S. gigantea. Our results indicate that host preference is not determined by a large number of genes because preference of hybrids did not correspond to the proportion of the genome derived from each host race. The strength of the ovipuncture preference for S. gigantea by gigantea females, the females of both reciprocal F1 hybrids, the backcross to gigantea, and F2s indicates that preference is inherited nonadditively at a limited number of loci. The F1 female hybrids, however, had a weaker host preference for S. gigantea than the pure gigantea host race, indicating that there may be incomplete dominance or modifier loci. Males had different host preference patterns than females, with individual male gigantea and male F1 hybrids usually exhibiting preference exclusively for S. gigantea or S. altissima. One hypothesis explaining the difference in host preference between males and females is that the same gene influences both female and male host preference, but it is a sex-influenced gene. Thus, males carrying the gene for S. gigantea preference have an intermediate host preference, whereas females have a strong host preference to S. gigantea. In summary, we found that the host preference that produces host-associated mating is inherited nonadditively at a relatively small number of loci on autosomal genes. This mode of inheritance meets the assumptions of models of sympatric speciation, indicating that the host races could have evolved in sympatry.     

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.     

Genetic isolation between two sympatric host-plant races of the European corn borer,Ostrinia nubilalis Hübner. I. Sex pheromone,moth emergence timing,and parasitism

Adaptation to different environments may be a powerful source of genetic differentiation between populations. The biological traits selected in each environment can pleiotropically induce assortative mating between individuals of these genetically differentiated populations. This situation may facilitate sympatric speciation. Successful host shifts in phytophagous insects provide some of the best evidence for the ecological speciation that occurs, or has occurred, in sympatry. The European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae), colonized maize after its introduction into Europe by humans about 500 years ago. In northern France, two sympatric host races feed on maize (Zea mays) and mugwort (Artemisia vulgaris), respectively. We investigated the factors involved in the genetic isolation of these two races at a field site near Paris, France. We identified two biological differences that might make a significant contribution to the genetic divergence between sympatric populations feeding on the two host plants. First, assortative mating may be due to differences in the moth emergence pattern between the two races: mugwort-race moths emerged on average 10 days earlier than maize-race moths. In addition, the males emerged earlier than females in both races. Hence, the likelihood of mating between maize-race males and mugwort-race females was higher than that of mating between mugwort-race males and maize-race females. Second, the females feeding on mugwort and maize produced sex pheromones with different E/Z isomeric ratios of delta-11-tetradecenyl acetate. This difference in mate recognition systems reinforces the potential for assortative mating in the two races. During the experiment, overwintering mortality was much lower on maize than on mugwort. This difference was due to a braconid parasitoid wasp, Macrocentrus cingulum, that killed more than 50% of the larvae overwintering on mugwort but did not infest larvae diapausing on maize. Hence, by colonizing maize, European corn borer populations probably escaped from numerous predators, competitors, and parasitoids, such as M. cingulum. This decrease in host-associated selection may have favored the colonization of this new host. Finally, throughout this experiment we observed selection at two allozyme loci (or at linked loci): Tpi and Mpi. The Tpi locus is tightly linked with the genes involved in the response of the male to the sex pheromone and in developmental timing. The location of these traits on the Z chromosome may play a role in shortening the time required for the evolution of premating barriers.     

Molecular evidence of host-associated genetic divergence in the holly leafminer Phytomyza glabricola (Diptera: Agromyzidae): apparent discordance among marker systems

Host races play a central part in understanding the role of host plant mediated divergence and speciation of phytophagous insects. Of greatest interest are host-associated populations that have recently diverged; however, finding genetic evidence for very recent divergences is difficult because initially only a few loci are expected to evolve diagnostic differences. The holly leafminer Phytomyza glabricola feeds on two hollies, Ilex glabra and I. coriacea, that are broadly sympatric throughout most of their ranges. The leafminer is often present on both host plants and exhibits a dramatic life history difference on the two hosts, suggesting that host races may be present. We collected 1393 bp of mitochondrial cytochrome oxidase I (COI) sequence and amplified fragment length polymorphism (AFLP) data (45 polymorphic bands) from sympatric populations of flies reared from the two hosts. Phylogenetic and frequency analysis of mitochondrial COI sequence data uncovered considerable variation but no structuring by the host plant, and only limited differentiation among geographical locations. In contrast, analysis of AFLP frequency data found a significant effect with host plant, and a much smaller effect with geographical location. Likewise, neighbour-joining analysis of AFLP data resulted in clustering by host plant. The AFLP data indicate that P. glabricola is most likely comprised of two host races. Because there were no fixed differences in mitochondrial or AFLP data, this host-associated divergence is likely to have occurred very recently. P. glabricola therefore provides a new sympatric system for exploring the role of geography and ecological specialization in the speciation of phytophagous insects.     

Host plant genotype influences survival of hybrids between Eurosta solidaginis host races

Extrinsic, host-associated environmental factors may influence postmating isolation between herbivorous insect populations and represent a fundamentally ecological cause of speciation. We investigated this issue in experiments on hybrids between the host races of Eurosta solidaginis, a fly that induces galls on the goldenrods Solidago altissima and S. gigantea. To do so, we measured the performance of parental host races and their hybrids on five genotypes of S. gigantea and nine genotypes of S. altissima to test hypotheses about how variation in plant genotype affects performance (i.e., fitness) and potentially influences gene flow between these host races. We found that rates of gall induction and of survival to adult emergence by hybrid larvae were significantly lower than those of both parental host races on both host species, adding support to the hypothesis that there is partial postmating isolation between the host races. Hybrid flies significantly varied in their performance across plant genotypes of both host species. A significant interaction between the effects of plant genotype and mating treatment (parental vs. hybrid crosses) on larval performance indicated that the relative suitability of particular plant genotypes differed between the parental host races and their hybrids. These patterns illustrate a poor correspondence between optimal parental and hybrid environments, consistent with the hypothesis that these host races are partially isolated due to extrinsic (ecological) factors. Based on these findings, we discuss the possibility that plant genotypes in which hybrid performance is high can facilitate hybridization and gene flow between partially reproductively isolated populations of herbivorous insects, thus affecting the dynamics of ecological speciation.     

Genetic differentiation among host-associated Alebra leafhoppers (Hemiptera: Cicadellidae)

The limited importance ascribed to sympatric speciation processes via host race formation is partially due to the few cases of host races that have been reported among host populations. This work sheds light on the taxonomy of Alebra leafhoppers and examines the possible existence of host races among host-associated populations. The species of this genus show varying degrees of host association with deciduous trees and shrubs and, frequently, host populations of uncertain taxonomic status coexist and occasionally become pests. Allozyme electrophoresis of 21 Greek populations including sympatric, local and geographically distant samples collected on 13 different plant species, show that they represent at least five species: A. albostriella Fallén, A. viridis (Rey) (sensu Gillham), A. wahlbergi Boheman and two new species. Of these, one is associated to Quercus frainetto and other is specific to Crataegus spp. Significant genetic differences among sympatric and local host populations were found only in A. albostriella, between populations on Turkey oak, beech and common alder. It is suggested that the last two of these host populations may represent different host races. The results show that both the host plant and geographical distance affect the patterns of differentiation in the genus. The formation of some species seems to have been the result of allopatric speciation events while, for others, their origin can be equally explained either by sympatric or allopatric speciation.     

Mitochondrial DNA variation among host races of Eurosta solidaginis Fitch (Diptera: Tephritidae)

Eurosta solidaginis Fitch (Diptera: Tephritidae) induces galls on two species of goldenrod, Solidago (Compositae), in the northern regions of the United States. Recent studies have demonstrated that E. solidaginis is comprised of two host races that differ in adult emergence times, mate preference, and host preference. However, it is not known how much genetic variation, if any, exists among E. solidaginis host-associated populations west of Minnesota where the two host races occur in sympatry. Sequencing analysis was used to characterize two mitochondrial gene fragments: (1) NADH1 dehydrogenase (ND1: 539 bp) and (2) cytochrome oxidase II + tRNA(Lys) + tRNA(Asp) (CO2KD: 396 bp) from sympatric, host-associated populations of E. solidaginis in North Dakota. Our results indicated that two genetically distinct lineages exist among E. solidaginis in North Dakota that correspond with host-plant association.     

Behavioural,ecological and genetic evidence confirm the occurrence of host‐associated differentiation in goldenrod gall‐midges

Host‐associated differentiation (HAD) is considered a step towards ecological speciation and an important mechanism promoting diversification in phytophagous insects. Although the number of documented cases of HAD is increasing, these still represent only a small fraction of species and feeding guilds among phytophagous insects, and most reports are based on a single type of evidence. Here we employ a comprehensive approach to present behavioural, morphological, ecological and genetic evidence for the occurrence of HAD in the gall midge Dasineura folliculi (Diptera: Cecidomyiidae) on two sympatric species of goldenrods (Solidago rugosa and S. gigantea). Controlled experiments revealed assortative mating and strong oviposition fidelity for the natal‐host species. Analysis of mitochondrial DNA showed an amount of genetic divergence between the two host‐associated populations compatible with cryptic species rather than host races. Lower levels of within‐host genetic divergence, gall development and natural‐enemy attack in the S. gigantea population suggest this is the derived host.     

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host‐associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host‐plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host‐associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe.     

The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis

1. A series of experiments was conducted to measure the impact of plant genotype, plant growth rate, and intraspecific competition on the oviposition preference and offspring performance of the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and Solidago gigantea (Asteraceae). Previous research has shown that both host races prefer to oviposit on their own host plant where survival is much higher than on the alternate host plant. In this study, neither host race showed any relationship between oviposition preference and offspring performance in choosing among plants of their natal host species. 2. The larval survival of both host races differed among plant genotypes when each host race oviposited on its natal host species. In one experiment, altissima host race females showed a preference among plant genotypes that was not correlated with offspring performance on those genotypes. In all other experiments, neither the altissima nor gigantea host race demonstrated a preference for specific host plant genotypes. 3. Eurosta solidaginis had a preference for ovipositing on rapidly growing ramets in all experiments, however larval survival was not correlated with ramet growth rate at the time of oviposition. 4. Eurosta solidaginis suffered high mortality from intraspecific competition in the early larval stage. There was little evidence, however, that females avoided ovipositing on ramets that had been attacked previously. This led to an aggregated distribution of eggs among ramets and strong intraspecific competition. 5. There was no interaction among plant genotype, plant growth rate, or intraspecific competition in determining oviposition preference or offspring performance.     

Host plant‐related genomic differentiation in the European cherry fruit fly,Rhagoletis cerasi

Elucidating the mechanisms and conditions facilitating the formation of biodiversity are central topics in evolutionary biology. A growing number of studies imply that divergent ecological selection may often play a critical role in speciation by counteracting the homogenising effects of gene flow. Several examples involve phytophagous insects, where divergent selection pressures associated with host plant shifts may generate reproductive isolation, promoting speciation. Here, we use ddRADseq to assess the population structure and to test for host‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi (L., 1758) (Diptera: Tephritidae). This tephritid is distributed throughout Europe and western Asia, and has adapted to two different genera of host plants, Prunus spp. (cherries) and Lonicera spp. (honeysuckle). Our data imply that geographic distance and geomorphic barriers serve as the primary factors shaping genetic population structure across the species range. Locally, however, flies genetically cluster according to host plant, with consistent allele frequency differences displayed by a subset of loci between Prunus and Lonicera flies across four sites surveyed in Germany and Norway. These 17 loci display significantly higher F_ST values between host plants than others. They also showed high levels of linkage disequilibrium within and between Prunus and Lonicera flies, supporting host‐related selection and reduced gene flow. Our findings support the existence of sympatric host races in R. cerasi embedded within broader patterns of geographic variation in the fly, similar to the related apple maggot, Rhagoletis pomonella, in North America.     

Geographic variation in the evolution and coevolution of a tritrophic interaction

The geographic mosaic theory of coevolution predicts that geographic variation in species interactions will lead to differing selective pressures on interacting species, producing geographic variation in the traits of interacting species (Thompson 2005). We supported this hypothesis in a study of the geographic variation in the interactions among Eurosta solidaginis and its natural enemies. Eurosta solidaginis is a fly (Diptera: Tephritidae) that induces galls on subspecies of tall goldenrod, Solidago altissima altissima and S. a. gilvocanescens. We measured selection on E. solidaginis gall size and shape in the prairie and forest biomes in Minnesota and North Dakota over an 11-year period. Galls were larger and more spherical in the prairie than in the forest. We supported the hypothesis that the divergence in gall morphology in the two biomes is due to different selection regimes exerted by natural enemies of E. solidaginis. Each natural enemy exerted similar selection on gall diameter in both biomes, but differences in the frequency of natural enemy attack created strong differences in overall selection between the prairie and forest. Bird predation increased with gall diameter, creating selection for smaller-diameter galls. A parasitic wasp, Eurytoma gigantea, and Mordellistena convicta, an inquiline beetle, both caused higher E. solidaginis mortality in smaller galls, exerting selection for increased gall diameter. In the forest there was stabilizing selection on gall diameter due to a combination of bird predation on larvae in large galls, and M. convicta- and E. gigantea-induced mortality on larvae in small galls. In the prairie there was directional selection for larger galls due to M. convicta and E. gigantea mortality on larvae in small galls. Mordellistena convicta-induced mortality was consistently higher in the prairie than in the forest, whereas there was no significant difference in E. gigantea-induced mortality between biomes. Bird predation was nonexistent in the prairie so the selection against large galls found in the forest was absent. We supported the hypothesis that natural enemies of E. solidaginis exerted selection for spherical galls in both biomes. In the prairie M. convicta exerts stabilizing selection to maintain spherical galls. In the forest there was directional selection for more spherical galls. Eurytoma gigantea exerted selection on gall shape in the forest in a complex manner that varied among years. We also supported the hypothesis that E. gigantea is coevolving with E. solidaginis. The parasitoid had significantly longer ovipositors in the prairie than in the forest, indicating the possibility that it has evolved in response to selection to reach larvae in the larger-diameter prairie galls.     

Phylogeographic patterns of host-race evolution in Tephritis conura (Diptera: Tephritidae)

Host-race evolution is a prime candidate for sympatric speciation because host shifts must take place in the presence of both hosts. However, the geographic context in which the shift takes place may have strong allopatric or peripatric components if the primary host within a localized area is scarce or even goes extinct. Inference of the relative importance of the geographic mode of speciation may be gained from phylogeographic imprints. Here, we investigate the phylogeography of host races of the tephritid fly Tephritis conura from sympatric, parapatric and allopatric populations of Cirsium heterophyllum and Cirsium oleraceum (Asteraceae) in Europe, for addressing the age and direction, and the geographic context of host-race formation. Haplotype networks of the host races differed significantly in molecular diversity and topology. However, host-race haplotypes were nested within the same network, with a central haplotype H1 being the most common haplotype in both host races. C. heterophyllum flies were genetically more diverse and substructured than flies from C. oleraceum, suggesting that the latter is the derived race. The phylogeographic imprint indicates either that C. heterophyllum flies colonized C. oleraceum during range expansion or that heterophyllum flies went extinct in an area where oleraceum flies persisted (followed by re-immigration). These imprints are in concordance with peripatric diversification, probably in the European Alps and related to the last ice age, where the host-race diversification was largely completed before the postglacial range expansion on C. oleraceum to current areas of sympatry and parapatry with C. heterophyllum.     

Sympatric host races of the European corn borer: adaptation to host plants and hybrid performance

The European corn borer (ECB), Ostrinia nubilalis, is a major pest of maize crops. In Europe, two sympatric host races are found: one feeds on maize (Zea mays) and the other mainly on mugwort (Artemisia vulgaris). The two host races are genetically differentiated, seldom crossing in the laboratory or in the field, and females preferentially lay eggs on their native host species. We conducted two independent experiments, in field and greenhouse conditions, to determine whether the two host races are locally adapted to their host species. The effect of larval density and the performance of hybrids were also investigated. Despite some differences in overall larval feeding performance, both experiments revealed consistent patterns of local adaptation for survival and for larval weight in males. In females the same trend was observed but with weaker statistical support. F1 hybrids did not seem to be disadvantaged compared with the two parental races. Overall, our results showed that both host races are physiologically adapted to their native host. The fitness trade-off between the two host plants provides a potential driving force for ecological speciation in this species.     

Host races in plant-feeding insects and their importance in sympatric speciation

The existence of a continuous array of sympatric biotypes - from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species - can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant-feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca. 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one-half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by-product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host-associated polymorphism to host-associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite-resistant plants.