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Evol Biol (2012) 39:219–230 DOI 10.1007/s11692-012-9182-7 SYNTHESIS PAPER Interspecific Competition and Speciation in Endoparasitoids Glen R. Hood • Scott P. Egan • Jeffrey L. Feder Received: 10 December 2011 / Accepted: 5 April 2012 / Published online: 20 April 2012 Springer Science+Business Media, LLC 2012 Abstract Ecological speciation occurs when inherent reproductive barriers to gene flow evolve between populations as a result of divergent natural selection. Frequency dependent effects associated with intraspecific resource competition are thought to be one important source of divergent selection facilitating ecological speciation. Interspecific competition may also play an important role in promoting population divergence. Although evidence for interspecific competition in nature is ubiquitous, there is currently little empirical data supporting its role in the speciation process. Here, we discuss two general models in which interspecific competition among species can promote ecological speciation among populations within a species. In both models, interspecific competition is the source of divergent selection driving adaption to different portions of the resource distribution, generating ecological reproductive isolation from other conspecific populations. We propose that the biology of endoparasitoids that attack phytophagous insects make model systems for studying the role of interspecific competition in ecological speciation. We describe details for one such system, the community of endoparasitic braconid wasps attacking Rhagoletis fruit flies, as a potential model for investigating competitive speciation. We conclude by hypothesizing that a model in which interspecific competition forces an inferior G. R. Hood (&) S. P. Egan J. L. Feder Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA e-mail: [email protected] S. P. Egan Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556, USA competitor to alternative fly hosts may be a common theme contributing to parasitoid diversification in the Rhagoletisparasitoid system. Keywords Braconid wasps Rhagoletis Ecological speciation Sequential speciation Cascading speciation Interspecific competition Divergent selection Introduction During the last 30 years, there has been increasing interest in the role that ecology plays in population divergence and speciation (Coyne and Orr 2004; Rundle and Nosil 2005; Funk et al. 2006). Much of this interest has come from empirical studies across various taxa (e.g., plants: Lowry et al. 2008; bacteria: Rainey and Travisano 1998; phytophagous insects: Funk et al. 2002; fishes: Schluter 2003; Bolnick and Preisser 2005), and from theoretical analyses showing that speciation can potentially occur in the absence of complete geographic isolation between populations (Dieckmann and Doebeli 1999; Kondrashov and Kondrashov 1999). In these cases, ecological speciation occurs when divergent adaptation to differences in local environmental conditions generates reproductive isolating barriers strong enough to overcome the homogenizing effects of gene flow (Schluter 2000a, 2001; Rundle and Nosil 2005). Specifically, ecological speciation is predicated on fitness tradeoffs in which a trait or characteristic of an organism make it better adapted to one environment and less well-suited for surviving and reproducing in alternative habitats. As a result, migrants will perform less well than resident individuals (Nosil et al. 2005) and hybrids will suffer reduced fitness compared to parental types in their respective natal habitats (Egan and Funk 123 220 2009; Egan et al. 2011), generating ecologically based reproductive isolation. Divergent ecological adaptation can stem, for example, from an organism’s quest to obtain food or nutrients, avoid predators, attract pollinators, or survive varying environmental conditions in alternate habitats (Rundle and Nosil 2005). Intraspecific resource competition has also been argued to be a common source for divergent selection (Rundle and Nosil 2005). Individuals within a population may often compete for limited resources. Thus, a trait that gives an individual a performance advantage to better garner resources should confer measurable fitness benefits over others lacking the trait. When resources are discrete in time, space, or physical characteristics such that different suites of traits are necessary to effectively utilize alternative resources, intraspecific competition can result in the evolution of ecologically specialized varieties or races within species, potentially leading to speciation (Rosenzweig 1978; Diehl and Bush 1989). Although less intuitively obvious, theoretical (Dieckmann and Doebeli 1999; Kondrashov and Kondrashov 1999) and empirical (Bolnick 2004; Bolnick and Lau 2008) studies have also suggested that the same may be true when resources are more continuously distributed. In this case, ecologically differentiated subpopulations can evolve due to frequency dependent effects resulting from intraspecific competition. These differences generate fitness tradeoffs in which individuals specialized for the most commonly used and, consequently, most depleted intermediate portion of the resource distribution, are at a disadvantage compared to individuals adapted to the extreme portions of the resource distribution (Rosenzweig 1978; Bolnick 2004). If traits involved in specialization become associated with assortative mating, then reproductive isolation can arise leading to ecological speciation (Schluter 2001; Gavrilets 2004). Although much of the focus on the role of resource utilization in speciation has centered on intraspecific competition, it has also been hypothesized that interspecific competitors could play an important role in population divergence (Rundle and Nosil 2005). If competition among conspecifics can generate sufficiently strong disruptive ecological selection pressures, then it stands to reason that similar considerations should also apply for interspecific taxa. However, while it is well established that interspecific competition occurs commonly in nature (Goldberg and Barton 1992; Gurevitch et al. 1992; Denno et al. 1995; Bolnick and Preisser 2005; Maestre et al. 2005; Kaplan and Denno 2007), the evidence for the involvement of interspecific competition in speciation is less clear. Here, we present two verbal models in which frequency dependent effects from interspecific competition can favor specialization for different aspects of the resource distribution, potentially triggering ecological speciation. We then 123 Evol Biol (2012) 39:219–230 examine why documenting a role for interspecific competition in the speciation process is difficult and discuss how endoparasitoids that attack phytophagous insects, and in particular the community of parasitoid wasps attacking Rhagoletis fruit flies, may be a test system for studying the consequences of interspecific competition for speciation. We conclude by proposing that a model in which interspecific competition between parasitoids forces an inferior competitor to alternative hosts may be a common theme contributing to parasitoid diversification in the Rhagoletisparasitoid system. Competition, Divergent Selection and Speciation The idea that competition can be an important factor facilitating speciation has a long history. In the Origin of Species, Darwin (1859, pp. 112, 121) originally hypothesized that intraspecific resource competition may lead to sympatric speciation via disruptive selection (Kondrashov and Kondrashov 1999). One of the first formal theoretical models of ‘competitive speciation’ was constructed by Rosenzweig (1978). In Rosenzweig’s model, frequency dependent effects of intraspecific competition generate a fitness landscape in which phenotypes using the more extreme portions of the resource distribution have increased fitness over intermediate phenotypes. Thus, a bimodal distribution of phenotypes representing two specialized subpopulations could evolve, that if coupled with a mechanism generating prezygotic isolation (e.g., by positive assortative mating based on phenotype or habitat preference), could result in sympatric ecological speciation. Variations on Rosenzweig’s theme of frequency dependent selection have subsequently been incorporated into several theoretical models of sympatric ecological speciation (Seger 1985; Doebeli 1996; Johnson and Gullberg 1998; Dieckmann and Doebeli 1999; Kondrashov and Kondrashov 1999; Doebeli and Dieckmann 2000, 2003; Drossel and McKane 2000; Kaneko 2002; Ackermann and Doebeli 2004; Brigatti et al. 2006; Burger et al. 2006; Pennings et al. 2008). Empirical studies have tested predictions regarding the frequency dependent effects of intraspecific competition across a wide range of organisms (e.g., bacteria: Rainey and Travisano 1998; insects: Bolnick 2001; fish: Schluter 2003). Specifically, it has been documented that (1) extreme phenotypes have evolved in experimental laboratory studies, (2) the abundance of intermediate resources have been found to be disproportionately depressed by resource competition, and (3) intermediate phenotypes have been shown to be most affected by resource competition. Together these findings are consistent with competitive speciation theory, however, no empirical study has yet to directly tie shifts in resource utilization due to Evol Biol (2012) 39:219–230 intraspecific competition to the evolution of reproductive isolation and speciation. 221 A Interspecific Competition and Speciation Ecological speciation could also potentially arise from divergent selection caused by interspecific competition between species. Similar to intraspecific competition, when individuals from different taxa share phenotypic features that cause them to overlap in their resource use, they will compete (Roughgarden 1972; Slatkin 1980; Taper and Case 1992; Doebeli 1996; Schluter 2000b). This can result in ecological character displacement, in which species diverge to utilize different aspects of the shared resource distribution where the taxa co-occur. Thus, displacement in one population can generate ecologically-based reproductive isolation with conspecifics elsewhere in the species range. We illustrate this scenario for speciation driven by interspecific competition in Fig. 1. Species 1 and 2 co-occur in habitat 1 and overlap in their use of an essential resource. Species 1 is also present in habitat 2, where species 2 is absent (Fig. 1a). We note that differences between habitats 1 and 2 can enhance ecological divergence, but it is not essential for competitive speciation. Frequency dependent effects of interspecific competition in habitat 1 result in species 1 evolving to use a different, extreme portion of the resource distribution (Fig. 1b). Figure 1c depicts the subsequent direct effects of ecological divergence for reproductive isolation. First, when individuals from habitat 1 migrate to habitat 2, they will suffer a fitness disadvantage compared to the residents in habitat 2 because they are confined to a less lucrative portion of the resource distribution. Second, individuals of species 1 migrating from habitat 2 to habitat 1 would suffer reduced fitness compared to residents due to competition from species 2. Third, in the absence of dominance effects, hybrids of intermediate phenotype would also be at a fitness disadvantage compared to parental types in both habitats 1 and 2. In addition to these direct ecological restrictions to gene flow, it is also possible for interspecific competition to generate intrinsic reproductive isolation as a pleiotropic by-product of ecological divergence if habitats 1 and 2 become geographically separated for a period of time. In this case, new favorable mutations established in species 1 in habitat 1 in allopatry can have negative epistatic effects on fitness in hybrids formed following secondary contact and migration between populations in habitat 1 and 2. Whether due to direct extrinsic or inadvertent intrinsic causes, reduced fitness of hybrids can favor the evolution of increased prezygotic isolation B C D Fig. 1 Model in which interspecific competition drives ecological character displacement between species 1 and species 2 in habitat 1, but not in habitat 2. Black and grey lines represent a distribution of phenotypes for species 1 and 2 across a resource gradient. Thus ecological displacement evolved by species 1 in habitat 1 can generate ecological-based reproductive isolation with conspecifics in habitat 2 upon secondary contact. See Section ‘‘Interspecific Competition and Speciation’’ for full description (reinforcement) between the populations in habitat 1 and 2 furthering the speciation process (Fig. 1d). Interspecific competition can also foster ecological divergence and speciation in a single habitat in a similar manner to the original Rosenzweig (1978) model. In this scenario, two species overlap in the use of a shared resource in habitat 1 (Fig. 2a). Species 2 is competitively superior to species 1, forcing it to adapt to the two extremes of the resource distribution in habitat 1 (Fig. 2b). As a result, two ecological races are formed in species 1 isolated by both the direct effects of disruptive selection in the two extreme resource tails and by hybrids with intermediate phenotypes being outcompeted by species 2 (Fig. 2c). 123 222 Evol Biol (2012) 39:219–230 A B C However, it is not clear how often interspecific competition leads to ecological speciation. At the time of their review Rundle and Nosil (2005) stated, ‘‘… as far as we are aware there are no direct tests, from nature or the laboratory, linking the evolution of reproductive isolation to interspecific competition.’’ One exception may be populations of the Mexican spadefoot toad (Spea multiplicata), which exist in the presence and absence of a competing species, the plains spadefoot toad (Spea bombifrons) (Pfennig and Rice 2007). The Mexican spadefoot toad conforms to a key prediction of interspecific competition: offspring derived from crosses between individuals from populations with S. bombifrons (i.e., within competitive environments) generally exhibited higher fitness (were larger in body size) than those derived from ‘‘hybrid’’ crosses between competitive environments and this effect was accentuated in a high versus low competition treatments. This is consistent with the model depicted in Fig. 1. Thus, in this example, postmating ecological isolation appears to have arisen as a by-product of interactions between species and molecular evidence suggests this may reduce gene flow between competitive environments (Rice and Pfennig 2010). Difficulties in Verifying a Role of Interspecific Competition in Speciation Fig. 2 Model in which interspecific competition fosters ecological divergence and speciation in a single habitat in a similar manner to the original Rosenzweig (1978) model. Black and grey lines represent a distribution of phenotypes for species 1 and 2 across a resource gradient. See Section ‘‘Interspecific Competition and Speciation’’ for full description Prezygotic reinforcement and eventually intrinsic reproductive isolation can evolve between the races furthering the speciation process. The Evidence for Interspecific Competition The effects of interspecific competition on adaptive divergence have been reviewed in detail elsewhere (Gurevitch et al. 1992; Denno et al. 1995; Schluter 2000b; Rundle and Nosil 2005). The general conclusion is that interspecific competition is common in nature and can play an important role in mediating species interactions and structuring communities for a diverse range of organisms (see Goldberg and Barton 1992 and Maestre et al. 2005 for plants; Gurevitch et al. 1992 and Bolnick and Preisser 2005 for examples across various taxa; Denno et al. 1995 and Kaplan and Denno 2007 for phytophagous insects). 123 Why is it difficult to verify a role for interspecific competition in speciation? We contend that the difficulties are due to (1) how current theory relates to the biology and natural history of populations and (2) empirical difficulties in studying competitive interactions. From a natural history perspective, there are reasons to suspect that intraspecific competition should be stronger than interspecific competition (Armstrong and McGhee 1980). After all, conspecific species share a common gene pool and recent common ancestry and are thus more phenotypically similar to one another than heterospecific species. Consequently, conspecifics will utilize resources in more similar manner across the entirety of niche space compared to individuals from different species. Thus, in terms of the strength of interactions, we might expect intraspecific competition to be a much stronger force promoting niche diversification and speciation than interspecific competition. Indeed, although species may a priori overlap greatly in their use of some resource dimensions, this may not be the case for others. As a result, species may often co-exist with little competitive selection pressure for ecological divergence unless the resource dimensions they share in common are essential for population persistence. Furthermore, when the resources are essential and interspecific competition strong, the consequence may be for competition to impede Evol Biol (2012) 39:219–230 ecological speciation through the local extinction of one species (i.e., filled niches do not allow for further species packing) (Bengtsson 1989). Thus, there are several biological criteria that must be met for interspecific competition to be a potential contributor to ecological speciation. First, with respect to the scenario for competitive speciation depicted in Fig. 1, the resource space in habitat 1 must be large enough to allow for both species 1 and 2 to persist. Second, the resources in habitat 1 must be sufficiently diverse such that it cannot be occupied and dominated competitively by pre-existing species 2 only. Third, the resource distributions of each species cannot be too dissimilar and at least one critical dimension must be shared extensively for the co-occurring species to compete. If competition is weak, then divergent ecological selection imposed on species 1 between habitats 1 and 2 divorced from the interspecific effects of species 2 will be the primary driver of population divergence. Fourth, fitness tradeoffs must exist if migration is occurring between habitats such that the differing ecologies experienced by species 1 in habitats 1 and 2 cannot be reconciled by a single phenotype and reproductive isolation evolves as a consequence of ecological adaptation. In short, the need for interspecific competition to be strong relative to intraspecific effects and for essential resources to be shared and of sufficient size and complexity to allow for co-existence and specialization may limit the opportunities for interspecific interactions to significantly contribute to ecological speciation in natural populations. The empirical difficulties and criteria for verifying a role for interspecific competition in ecological speciation have been discussed by Schluter (2000a, b) and we highlight several problems here. One difficulty is that the primary observational pattern of ecological character displacement used to infer interspecific competition could be due to other causal factors besides competition. Ecological character displacement is a pattern in which divergence between species is greater when they co-occur together (i.e., sympatry = interspecific competition present) compared to when they do not (i.e., allopatry = interspecific competition absent) (Pfennig and Pfennig 2005; Rice and Pfennig 2010). This pattern could reflect the direct consequences of interspecific competition shifting the ecologies of species to reduce resource overlap in the area of sympatry. However, to confirm competition as an important source of disruptive selection, it must be shown to generate differences beyond those expected by the resource distributions alone. Thus, environmental differences between allopatric and sympatric sites must be controlled and accounted for, as differences in environmental conditions in sympatry, irrespective of the presence of the additional taxon, could also explain a pattern of ecological character displacement. Moreover, reinforcement could be a complicating factor 223 when co-occurring species are evolutionarily closely related such that heterospecific individuals court and mate. When interspecific matings are only partly fertile and hybrids inviable or sterile, increased prezygotic isolation between populations can evolve to minimize fitness loss associated with wasted energy expended in courtship, gamete production, and hybrids formation (Rundle and Nosil 2005). When ecology affects the potential for crossmating, differences that evolve that appear to be due to divergent natural selection could instead be favored as a consequence of the increased degree of conspecific assortative mating they produce (Rundle and Nosil 2005). Resolving these causal factors can be difficult because selection pressures for reinforcement will coincide with those of interspecific competition, being present in sympatry where taxa co-occur and absent in allopatry where only one taxon is present (Schluter 2001). We hypothesize that one possible distinguishing feature may be that interspecific competition may often be intense across all life history stages, including juvenile stages, while ecological reinforcement may be most pronounced for sexually mature adults. The above considerations make it important to obtain independent evidence that similar phenotypes compete for resources to verify the causal basis inferred from observational patterns of ecological character displacement (Schluter 2000a, b). Perhaps the strongest independent evidence can come from laboratory and field experiments in which both conspecific and heterospecific individuals from allopatric and sympatric study sites are reared in different combinations under varying environmental conditions to tests for measurable effects of interspecific competition on the resource distribution and fitness of species (see the spadefoot toad example above). A corollary of this approach for species displaying varying degrees of character displacement or putative ecological divergence is that the effects of interspecific competition should diminish for species showing more and pronounced character differences for key traits as they diverge (Prichard and Schluter 2001; Gray and Robinson 2002). Finally, even if interspecific competition is experimentally demonstrated, it remains to be shown that the resulting ecological displacement generated in sympatry generates reproductive isolation from other conspecific populations if competition is contributing to speciation. This is a difficult task that may require a combination of crossing and reciprocal rearing studies to verify reduced hybrid fitness, as well as genetic surveys of natural populations. The latter would be greatly aided if (1) a mosaic of populations with and without competitors was arrayed across the landscape and (2) the genetic basis for traits involved in ecological character displacement are known and quantitative trait loci (QTL) mapped in the genome. 123 224 If this is the case, genome scans can test the prediction that local demes separated by comparable geographic distances and experiencing similar competitive environments (with or without competitors) should show higher levels of gene flow (be more genetically similar) than demes that differ. Moreover, effective gene flow should be reduced between demes with and without competitors around regions of the genome containing QTL for ecologically diverged traits (Nosil et al. 2009). Ideal Attributes for Study Systems Based on the above discussion, attributes of certain systems can make them more amenable to testing if and how interspecific competition contributes to speciation. Ideally, it would be convenient to work on a closed system in which the ecology can be circumscribed by a given resource shared by a clearly demarked group of organisms. Thus, all the interacting players rely solely on the resource for survival and influence by outside factors is minimized. In a closed system, competition is direct and most easily measured if it results in the death of one competitor and survival of another. Furthermore, it is important that although the system may be closed and easily defined, the key resource can be partitioned and is not uniformly distributed across space, time or some other aspect of the environment. It is also helpful when sympatric sites possessing competitors and allopatric sites lacking competitors are arrayed in a patchwork across the landscape. This allows one to (1) verify that predicted patterns of ecological character displacement exists, (2) conduct transplant experiments involving relocating individuals among sites to test whether competition occurs and is associated with the key traits displaying character displacement, and (3) perform genetic surveys to determine if gene flow is reduced between populations differing in competitive environments. Finally, systems that are amendable to manipulation in the laboratory have the added benefits of controlling the competitive environment to test for fitness effects during interspecific interactions, as well as the ability to perform crosses to genetically map adaptive traits and assess hybrid performance, further demonstrating ecological reproductive isolation. Endoparasitic Insects as Models for Competitive Speciation Several attributes make parasitic insects (parasitoids) model systems for testing for competitive speciation. First, there are a large number of parasitoid species to test for interspecific competition distributed across five different 123 Evol Biol (2012) 39:219–230 orders: Coleoptera, Diptera, Lepidoptera, Hymenoptera and Neuroptera (Godfray 1994). Collectively, parasitoids are extremely diverse, accounting for an estimated 20 % of all insect species. One group, parasitic wasps (Hymenoptera), is particularly species-rich, comprising 20 % of all insect parasitoids worldwide (La Salle and Gauld 1991). Thus, documenting competitive speciation in parasitoids, especially wasps, would imply that the process is an important general contributor to biodiversity, at least in terms of raw numbers of species generated. Second, endoparasitoids spend the immature stages of their life cycle (larval stage) internally feeding and developing to adulthood within a single host organism, typically killing their host in the process (Godfray 1994). Thus, parasitoids are confined to a closed resource essential for survival constituting a closed arena for which interspecific competition can take place. In addition, the majority of parasitoids are host specific at the genus or species level (Godfray 1994) and commonly overlap within individual hosts (Hawkins and Lawton 1987). Thus, competition cannot be easily diffused by a parasitoid using a novel insect host in an area where overlap with other parasitoids sharing the same primary host exists. Moreover, when multiparasitism occurs, it is typical for only one parasitoid to emerge victorious (Godfray 1994). Interspecific competition is therefore direct between endoparasites and has a clear outcome. Indeed, interspecific competition has been documented for many systems. In a literature search on Web of Science (Thompson Reuters) using the search terms ‘interspecific’, ‘competition’, and ‘parasitoid’, we documented [150 empirical studies demonstrating interspecific competition between the larval stages of two or more species of endoparasitoids attacking over 75 different species of plant-feeding insects. Consequently, there is little doubt that interspecific competition is common among endoparasitoids during larval development. Third, although the insect host is a closed system, it can still be potentially partitioned by life stage, space, and time to allow for ecological differentiation and competitive speciation in endoparasitoids. Specifically, egg, larva, pupa and adult life stages can represent different host niches for specialization requiring different sets of characteristics from competing species to effectively attack (Godfray 1994). Also, these life stages can vary in abundance and vulnerability temporally and (or) spatially across an environment. Fourth, many endoparsitoid systems are amenable to manipulation in the laboratory and field. This can allow for independent experimental evidence to be obtained to qualitatively confirm competition and for details of the effects of competition to be quantified. For example, by manipulating the order, life stage, or location that a host is exposed to parasitism, one could test for the presence of a Evol Biol (2012) 39:219–230 competitive hierarchy among endoparasites (e.g., is the first species to parasitize a host always victorious or is there a consistent competitive dominance of one species over another or is one species a superior competitor in one host life stage and inferior in others). In addition, trait values can also be potentially varied between competitors to test if specific characters alleviate competition between interspecific species in sympatry and generate ecological reproductive isolation between conspecific species. Finally, endoparasitoid species often have patchy distributions on local and regional scales. As a result, natural and independent replicates of competing parasitoid species exist at the population level both allopatrically and sympatrically. Spatial variation allows for comparisons to be made of the realized niches of different species in the presence and absence of interspecific competitors to test for patterns of ecological character displacement. Furthermore, allopatric and sympatric populations of species arrayed across the landscape provide replicates to genetically test if gene flow is reduced between populations differing in competitive environments. The Braconid Parasitoids of Rhagoletis Fruit Flies Recently, we have been studying the host specific endoparasitoid wasp community (Hymenoptera: Braconidae) that attacks Rhagoletis fruit flies (Diptera: Tephritidae) as a potential model for testing the role of interspecific competition in speciation. The Rhagoletis-parasitoid system has several attributes that make it amenable to study. First, flies in the Rhagoletis pomonella complex have adaptively radiated onto a number of different plants in North America including hawthorn (Crataegus spp.), snowberry (Symphoricarpos spp.), blueberry (Vaccinium spp.), flowering dogwood (Cornus florida) and silky dogwood (Cornus amomum), forming a series of sibling species and ecological races in the process (Bush 1966; Berlocher et al. 1993; Feder et al. 1994). Most famously, the recent shift *150 years ago of R. pomonella from its ancestral host the downy hawthorn (C. mollis) to introduced, domesticated apple (Malus domestica) in the Eastern United States is often cited as an example of sympatric speciation in action (Feder et al. 1988). Thus, there exists a bevy of potential host fly resources available for parasitoids to attack and specialize on–some of which have a well-documented recent origin–providing a number of potential examples to test whether and how the presence or absence of parasitoid competitors affects the potential for ecological diversification. The second attribute is that the life cycle of each parasitoid mirrors that of their fly host. Like Rhagoletis, each parasitoid species typically has one generation per year. 225 Wasps, like flies, mate on or near their host fruit. Female wasps will examine the surface of a host fruit with their antennae to detect and then directly oviposit into a fly egg or larva in the fruit (Lathrop and Newton 1933). When fruit fall to the ground, fly larvae leave the fruit, burrow into the soil, and pupate. The wasp egg will then hatch and the larva will consume its host and develop inside the fly puparium. The following summer wasps will eclose as adults. Parallels in life history translate to similarities in the ecology between flies and parasitoids. In particular, differences in diapause timing and host fruit odor discrimination are important ecological adaptations involved in host plant shifting and speciation for Rhagoletis. Diapause timing is important because flies are univoltine and have a short life span, thus adults must phenologically synchronize eclosion to the availability of ripe host fruit to maximize fitness (Feder et al. 1993, 1994). In addition, Rhagoletis use the volatile compounds emitted from the surface of ripening fruit as olfactory cues to locate and discriminate host plants (Linn et al. 2003; Forbes et al. 2005). This is particularly important as adult flies use host fruit as rendezvous sites for mating. The parasitoids of Rhagoletis likely experience similar divergent selection pressures on diapause life history timing and host fruit odor discrimination (for one species, Diachasma alloeum, this has been documented; see below). Parasitoid eclosion phenology must be synchronized with the phenology of fly development in fruits to ensure maximum resource availability. Also, because each species of wasp has a free living, sexual adult stage, and mate on or near their host fruit, host odors are also likely used to locate and discriminate host plants. Consequently, these shared characteristics highlight ecological that are critical for host-related specialization contributing to reproductive isolation and speciation and are candidates for ecological character displacement. When Rhagoletis flies shift and adapt to a new host plant they create a new niche and opportunity for their host specific parasitoids to follow suit and speciate in kind. If the life cycles and ecologies of organisms are linked, and similar characteristics are under divergent selection, speciation by one organism can drive similar diversification of associated organisms in adjacent trophic levels in a term coined sequential speciation. Forbes et al. (2009) documented sequential speciation among populations of D. alloeum, an endoparasitoid attacking flies in the R. pomonella complex, which is diverging in parallel with its fly host, forming genetically and ecologically diverging incipient host races. Paralleling their fly hosts, sympatric populations of D. alloeum attacking apple, hawthorn, and blueberry flies differ in microsatellite allele frequencies, diapause timing and host odor discrimination. Evidence for sequential speciation in D. alloeum shows parasitoids can diversify through ecological means, with the critical 123 226 Evol Biol (2012) 39:219–230 divergent selection pressures cascading up trophic levels in the ecosystem from plant to fly to parasitoid. It remains to be seen if similar processes are affecting the remaining members of the parasitoid community and if ecological divergence is being accentuated by interspecific competition. However, the possibility exists, as a clear connection can be made between ecological adaptation and reproductive isolation for D. alloeum and competitive interactions have been documented between all three species (see below). The third attribute is that interspecific competition exists for a limited resource in the larval stage of the parasitoid life cycle. At least three genera of host specific parasitoids attack flies in the R. pomonella complex, Utetes, Diachasmimorpha, and Diachasma (Forbes et al. 2010). Furthermore, each species attacks a different life stage of its fly host (Table 1). Utetes oviposit into fly eggs while Diachasma and Dichasmimorpha attack 2nd and 3rd instar larvae. Dissection and genetic analysis have indicated that Rhagoletis flies are often parasitized by more than one species of wasp (Lathrop and Newton 1933; G. Hood et al. unpublished). For example, in a genetic survey of 104 hawthorn-origin flies from Fennville, MI, analyzed shortly after puparium formation using species–specific mtDNA markers, we found an overall parasitism rate of 65 %, with 7.5 % of hosts being multi-parasitized by at least two, and in one case three different parasitoid species. Moreover, only one species at most has ever been observed to eclose from a fly puparium and upon emergence the fly pupa and any other parasitoid rivals are completely consumed (Lathrop and Newton 1933). Thus, there is clear evidence for direct interactions among endoparasitoids of Rhagoletis flies for a critical and limited resource. How does competition manifest itself between species? One common mechanisms of competitive interaction between parasitoids is physical attack. Lathrop and Newton (1933) observed that 1st instar larvae of D. alloeum (= O. malleus) have mandibular mouthparts used for fighting. Parasitoids with ‘fighting mandibles’ have been shown to have a competitive advantage over species with succulent mouthparts during direct combat (Harvey and Partridge 1987; Harvey et al. 2000; van Nouhuys and Punju 2009). Consequently, the presence of mandibles in D. alloeum implies that Rhagoletis parasitoids engage in direct combat as larvae, although it remains to be determined whether Utetes and (or) Diachasmimorpha possess mandibular mouthparts as well. The fourth attribute concerns the geographic distributions and host associations of Rhagoletis-attacking parasitoids. On a local scale in the Eastern U.S., surveys Table 1 Host associations and geographic locations for each member of the Rhagoletis pomonella sibling species complex and its associated community of braconid parasitoid wasps in the Northeastern (NE), Midwestern (MW) and Southern (S) USA Rhagoletis species Host plant Common name Attacking parasitoid spp. Relative abundance Location R. pomonella Crataegus spp. Hawthorn D. alloeum High NE, MW D. mellea Low NE, MW U. canaliculatus Low NE, S U. lectoides Low MW D. alloeum High NE, MW D. mellea Low NE, MW U. canaliculatus Low NE U. lectoides Low MW D. alloeum Rare NE D. mellea Medium MW U. canaliculatus High NE D. alloeum High NE D. mellea Low NE, Sa R. pomonella R. nr. pomonella R. mendax R. zephyria R. cornivora Malus pumila Cornus florida Vaccinium spp. Symphoricarpos spp. Cornus amomum Apple Flowering dogwood Blueberry Snowberry Silky dogwood Detailed distributions of each species are given in Forbes et al. (2010) a Species is rare in that specific geographic location 123 U. richmondii Low NE, S D. alloeum D. mellea Rare Medium NE NE U. canaliculatus High NE U. lectoides Low MW U. canaliculatus High NE Evol Biol (2012) 39:219–230 indicate a patchwork pattern of parasitism across the landscape. At the majority of sites, D. alloeum is the most abundant parasitoid attacking hawthorn, apple and blueberry flies, followed by Utetes canaliculatus and then Diachasmimorpha mellea (Table 1) (Forbes et al. 2010). This pattern suggests that D. alloeum attacking hawthorn, apple, and blueberry flies may be competitively superior. For related species attacking flowering dogwood, silky dogwood, and snowberry flies, U. canaliculatus is the numerically dominant while D. alloeum is less abundant or absent (Table 1). On a regional level in the Southern United States D. alloeum is uncommon (Table 1). Spatial variation in host associations of parasitoids therefore allow for comparisons to be made of the realized niches for different species in the presence and absence of interspecific competitors to test for ecological character displacement. We predict that competition should have more dramatic effects between larval-attacking parasitoid (D. alloeum and D. mellea) compared to egg-attacking parasitoids (Utetes). Consistent with this prediction, on a common apple, hawthorn and blueberry host, D. alloeum predominates, while on flowering dogwood, silky dogwood, and snowberry flies, D. mellea is more common. In comparison, Utetes is more uniform in its density across hosts (Table 1). Consequently, coexistence may be permitted because the host is vulnerable at different life stages that require mutually exclusive adaptations to parasitize. For example, adult parasitoids attacking fly eggs must eclose earlier while parasitoids attacking 2nd and 3rd instar larvae must eclose later. Thus, if egg-attacking parasitoids are superior in direct competition with larval-attacking parasitoids because they are first to attack hosts, for example, they may not be able to numerically supplant the larval-attacking parasitoids due to the narrow temporal window that eggs are vulnerable to parasitism (*48 h) (Feder 1995). Therefore, if we are seeking to detect interspecific effects on population divergence on a common resource as depicted in Figs. 1 and 2, then it would seem that Diachasma and Diachasmimorpha are the best targets for study. The structure of the egg-parasitoid community implies that competition may preclude multiple egg-attacking wasps from using the same host in a common area. Three egg-attacking parasitoid species, U. canaliculatus, U. richmondi, and U. lectoides, attack species within the genus Rhagoletis. These include U. canaliculatus and U. richmondi, which are sympatric across most of their respective ranges, however, they do not overlap in host species attacked (Forbes et al. 2010). Moreover, U. lectoides is isolated by distance from U. canaliculatus and U. richmondi. Thus, egg–attacking parasitoids do not co-occur on the same host in a given geographic area, implying that the egg resource may be too limited to 227 support multiple species. As a consequence, the absence of other egg-attacking parasitoids may be a prerequisite for successful host shifting and race formation in Utetes. Despite the apparent constricting effects that competition among U. lectoides, U. canaliculatus, and U. richmondi place on diversification, it is still conceivable that interspecific interactions among parasitoids have creative consequences for speciation. Specifically, instead of being limited to one fly species, the host resource may be a bi-modal distribution of two Rhagoletis species (fly 1 and fly 2), with fly 1 being a more optimal resource. Again, competition excludes the inferior egg–attacking parasitoid species 1 from the more optimal host 1 where the eggattacking parasitoid 1 and 2 overlap. However, in other geographically areas lacking fly 2 and parasitoid species 2, parasitoid 1 is free of competition and utilizes fly host 1 exclusively. It is therefore possible that competition played a role in fostering divergence if the population of parasitoid species 1 in the non-overlapping region was ancestral and colonized the area where parasitoid species 2 is present. Competition then forced parasitoid 1 to shift to fly host 2, resulting in subsequent adaptive changes that potentially reproductively isolate it from the ancestral population attacking fly host 1. Similar considerations may also apply to larval-attacking parasitoids. If it can be shown that (1) Diachasmimorpha attack flies in the South where Diachasma is rare, (2) Diachasmimorpha is largely excluded by Diachasma in the North, (3) flies attacked by Diachasmimorpha in the Northeast are either not present or not attacked in the South, (4) adaptation to the new fly host(s) in the Northeast generated reproductive isolation, and (5) southern populations of Diachasmimorpha are ancestral, competition likely played a role in host shifting events. The latter point is important because it is also possible that Diachasmimorpha form the North migrated southward and took advantage of the open fly resource niche in that area. In this case, rather than competition fostering speciation, it was the release from interspecific competition that allowed for divergence. Blueprint for Future Studies Details of the Rhagoletis-parasitoid system provide good evidence that interspecific competition is occurring for a limited resource. Support also exists for sequential host race formation and speciation in Diachasma alloeum (Forbes et al. 2009). Thus, differential ecological adaptation to Rhagoletis hosts can drive diversification at the higher trophic level. It remains to be seen if similar cascading ecological considerations apply to Utetes and Diachasmimorpha. This will require genetic surveys and tests for diapause and host odor discrimination behaviors to 123 228 Evol Biol (2012) 39:219–230 confirm the existence of ecologically specialized parasitoid taxa attacking different Rhagoletis hosts. If sequential divergence is found throughout the parasitoid community, then the next issue is to assess if interspecific competition played a role in facilitating the observed patterns of adaptive radiation. To accomplish this, we need to expand mtDNA analysis to accurately quantify levels of interspecific competition (e.g., what proportion of flies are multiply parasitized by different species) and whether a competitive hierarchy exists among taxa. Presently, the major attribute lacking for the Rhagoletis-parasitoid system is that we cannot rear large numbers of the parasitoids in the laboratory to perform manipulative experiments. While we are working on improving this aspect of parasitoid husbandry, related Diachasmimorpha and Utetes species can be reared in mass on the Mexican fruit fly, Anastrepha ludens (Ovruski et al. 2000). Thus, it is possible to conduct manipulative rearing experiments on related species to assess several assumptions outlined above. Surveys will then be required to determine whether ecological character displacement is occurring through comparisons of sites where competitors are both allopatric and sympatric. In this regard, aspects of the natural history and distributions of Diachasma, Diachasmimorpha, and Utetes suggest that subdivision of a shared host resource may not be the only or primary means by which interspecific competition is fostering divergence. In addition, it is possible that competition between species attacking the same life stage of a shared host exerts selection pressures on the inferior species to shift and adapt to a secondary Rhagoletis host that is not utilized. Thus, interspecific competition may constrain diversity within fly hosts, but still acts creatively by forcing radiation of parasitoids onto alternative fly hosts locally. Testing this hypothesis will entail confirming that populations attacking alternate hosts represent evolutionarily derived populations that are genetically differentiated and owe their reproductive isolation to ecological adaptations resulting from host shifts imposed upon them by competitors present on the ancestral host. Finally, intraspecific crosses can also be performed with the related species described above to allow for genetic analysis and marker mapping. While not ideal, the ability to experimentally and genetically manipulate species related to Rhagoletisattacking parasitoids will produce results relevant to discerning the role interspecific competition plays in ecological speciation. Denno et al. 1995; Bolnick and Preisser 2005; Maestre et al. 2005; Kaplan and Denno 2007). These ideas have influenced the longstanding view that, given the proper set of ecological conditions, intraspecific competition can facilitate speciation (Rundle and Nosil 2005). However, it is not definitively established whether interspecific competition plays a significant role in creating new biodiversity by fostering ecological divergence and speciation. While empirical studies have supported patterns of ecological character displacement driven by interspecific interactions (Pfennig and Pfennig 2009), to confirm that competition is an important source of divergent selection driving ecological differentiation, it must be shown to generate differences beyond those expected by the resource distributions alone. Moreover, this accentuation of ecological differentiation must be linked to the evolution of reproductive isolation to confirm competitive speciation. It is the latter connection that has not been convincingly made. Herein, we contend that the host specific endoparasitoid communities of phytophagous insect have several attributes that make them models for investigating the role that interspecific competition plays in the speciation process. Patterns of species overlap between members of the endoparasitoid community that attack Rhagoletis fruit flies imply that rather than biodiversity being generated exclusively by subdividing a shared host resource, interspecific competition may exert its effects on speciation by forcing taxa to shift and adapt to alternate, underused hosts in areas of species overlap. Subsequent adaptation to the new, derived host is the source for ecological reproductive isolation in this scenario. This hypothesis can be tested, but will require the application of a combination of field, laboratory, and genetic approaches to do so. Perhaps most significantly, advances in next generation DNA sequencing and massively parallel genotyping will allow comprehensive surveys of the genome to estimate levels of gene flow, identify genomic regions under divergent selection and map traits associated with ecological adaptation linking the evolutionary responses to interspecific competition to reproductive isolation and speciation. Conclusions References Competition is common in nature and competitive interactions help shape the structure and composition of communities (Goldberg and Barton 1992; Gurevitch et al. 1992; Ackermann, M., & Doebeli, M. (2004). Evolution of niche width and adaptive diversification. Evolution, 58, 2599–2612. Armstrong, R. A., & McGhee, R. (1980). Competitive exclusion. American Naturalist, 115, 151–170. 123 Acknowledgments GRH would like to thank P. Morton for continuous support and SPE would like to thank J. L. Greene for permanent support. JLF and GRH would like to thank Mazatlan in Pendleton, OR. 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