Explore the vast range of titles available.

Phenotypic and genetic variation in one species can influence the composition of interacting organisms within communities and across ecosystems. As a result, the divergence of one species may not be an isolated process, as the origin of one taxon could create new niche opportunities for other species to exploit, leading to the genesis of many new taxa in a process termed “sequential divergence.” Here, we test for such a multiplicative effect of sequential divergence in a community of host-specific parasitoid wasps,Diachasma alloeum, Utetes canaliculatus, andDiachasmimorpha mellea(Hymenoptera: Braconidae), that attackRhagoletis pomonellafruit flies (Diptera: Tephritidae). Flies in theR. pomonellaspecies complex radiated by sympatrically shifting and ecologically adapting to new host plants, the most recent example being the apple-infesting host race ofR. pomonellaformed via a host plant shift from hawthorn-infesting flies within the last 160 y. Using population genetics, field-based behavioral observations, host fruit odor discrimination assays, and analyses of life history timing, we show that the same host-related ecological selection pressures that differentially adapt and reproductively isolateRhagoletisto their respective host plants (host-associated differences in the timing of adult eclosion, host fruit odor preference and avoidance behaviors, and mating site fidelity) cascade through the ecosystem and induce host-associated genetic divergence for each of the three members of the parasitoid community. Thus, divergent selection at lower trophic levels can potentially multiplicatively and rapidly amplify biodiversity at higher levels on an ecological time scale, which may sequentially contribute to the rich diversity of life.

The enemy release hypothesis (ERH) predicts that the success of invasive species is caused by reduced enemy pressure in species’ introduced ranges. The ERH is a highly-cited explanation for invasion success, yet rigorous evidence is lacking for most species and ecosystems. Most evidence comes from observations of enemies in native and introduced ranges. These studies assess one aspect of the ERH—“enemy loss.” They do not provide a direct test of the ERH and overlook the assumption of “native enemy effects.” This is a critical limitation as enemy release will not occur if enemies do not affect species in their native ranges, even if enemy loss occurs. Biogeographical experiments, providing a direct test of the ERH, are largely restricted to terrestrial plants. We present a synthesis of community ecology and invasion biology studies, including a novel meta-analysis of native enemy effects, to assess the potential for release for species in different taxonomic groups and ecosystems. We suggest that species that are subject to strong enemy effects in their native range will have a high potential for enemy release. We found that native enemy effects were stronger in aquatic systems than in terrestrial systems. They were particularly weak for terrestrial plants; and strong for marine organisms, and freshwater plants. Studies are needed for species that have strong potential for release, such as for aquatic invasive species. Alternative explanations should be explored for invasive species that are not affected by enemies in their native range, and future studies should emphasize native enemy effects rather than only enemy loss.

A major cause for biodiversity may be biodiversity itself. As new species form, they may create new niches for others to exploit, potentially catalyzing a chain reaction of speciation events across trophic levels. We tested for such sequential radiation in the Rhagoletis pomonella (Diptera: Tephritidae) complex, a model for sympatric speciation via host plant shifting. We report that the parasitic wasp Diachasma alloeum (Hymenoptera: Braconidae) has formed new incipient species as a result of specializing on diversifying fly hosts, including the recently derived apple-infesting race of R. pomonella. Furthermore, we show that traits that differentially adapt R. pomonella flies to their host plants have also quickly evolved and serve as ecological barriers to reproduction, isolating the wasps. Speciation therefore cascades as the effects of new niche construction move across trophic levels.

Speciation with gene flow is expected to generate a heterogeneous pattern of genomic differentiation. The few genes under or physically linked to loci experiencing strong disruptive selection can diverge, whereas gene flow will homogenize the remainder of the genome, resulting in isolated \"genomic islands of speciation.\" We conducted an experimental test of this hypothesis in Rhagoletis pomonella, a model for sympatric ecological speciation. Contrary to expectations, we found widespread divergence throughout the Rhagoletis genome, with the majority of loci displaying host differences, latitudinal clines, associations with adult eclosion time, and within-generation responses to selection in a manipulative overwintering experiment. The latter two results, coupled with linkage disequilibrium analyses, provide experimental evidence that divergence was driven by selection on numerous independent genomic regions rather than by genome-wide genetic drift. \"Continents\" of multiple differentiated loci, rather than isolated islands of divergence, may characterize even the early stages of speciation. Our results also illustrate how these continents can exhibit variable topography, depending on selection strength, availability of preexisting genetic variation, linkage relationships, and genomic features that reduce recombination. For example, the divergence observed throughout the Rhagoletis genome was clearly accentuated in some regions, such as those harboring chromosomal inversions. These results highlight how the individual genes driving speciation can be embedded within an actively diverging genome.

Chromosomal inversions are ubiquitous in nature and of great significance for understanding adaptation and speciation. Inversions were the first markers used to investigate the genetic structure of natural populations, leading to the concept of coadapted gene complexes and theories concerning founder effects and genetic drift in small populations. However, we still lack elements of a general theory accounting for the origins and distribution of inversions in nature. Here, we use computer simulations to show that a \"mixed geographic mode\" of evolution involving allopatric separation of populations followed by secondary contact and gene flow generates chromosomal divergence by natural selection under wider conditions than previous hypotheses. This occurs because inversions arising in allopatry contain a full complement of locally adapted genes. Once gene flow ensues, reduced recombination within inversions keeps these favorable genotypic combinations intact, resulting in inverted genomic regions being favored over collinear regions. This process allows inversions to establish to high frequencies. Our model can account for several classic patterns in the geographic distribution of inversions and highlights how selection on standing genetic variation allows rapid chromosomal evolution without the waiting time for new mutations. As inversion differences often separate closely related taxa, mixed modes of divergence could be common.

The apple maggot fly , Rhagoletis pomonella , infests apple ( Malus domestica ) and hawthorn species (most notably the downy hawthorn, Crataegus mollis ) in the eastern USA. Evidence suggests that the fly was introduced into the western USA sometime in the last 60 years. In addition to apple, R. pomonella also infests two species of hawthorns in the western USA as major hosts: the native black hawthorn ( C. douglasii ) and the introduced ornamental English hawthorn, C. monogyna . Apple and downy hawthorn-origin flies in the eastern USA use volatile blends emitted from the surface of their respective ripening fruit to find and discriminate among host trees. To test whether the same is true for western flies, we used coupled gas chromatography and electroantennographic detection (GC-EAD) and developed a 7-component apple fruit blend for western apple-origin flies, an 8-component black hawthorn fruit blend for flies infesting C. douglasii , and a 9-component ornamental hawthorn blend for flies from C. monogyna . Crataegus douglasii and C. monogyna -origin flies showed similar levels of upwind directed flight to their respective natal synthetic fruit blends in flight tunnel assays compared to whole fruit adsorbent extracts, indicating that the blends contain all the behaviorally relevant fruit volatiles to induce maximal response levels. The black and ornamental hawthorn blends shared four compounds in common including 3-methylbutan-1-ol, which appears to be a key volatile for R. pomonella populations in the eastern, southern, and western USA that show a preference for fruit from different Crataegus species. However, the blends also differed from one another and from domesticated apple in several respects that make it possible that western R. pomonella flies behaviorally discriminate among fruit volatiles and form ecologically differentiated host races, as is the case for eastern apple and hawthorn flies.

The apple maggot fly , Rhagoletis pomonella , infests several hawthorn species in the southern USA. Here, we tested the hypothesis that these populations could serve as reservoirs for fruit odor discrimination behaviors facilitating sympatric host race formation and speciation, specifically the recent shift from downy hawthorn ( Crataegus mollis ) to domestic apple ( Malus domestica ) in the northern USA. Coupled gas chromatography and electroantennographic detection (GC-EAD), gas chromatography with mass spectrometry (GC-MS), and flight tunnel bioassays were used to identify the behaviorally active natal fruit volatile blends for three of the five major southern hawthorns: C. opaca (western mayhaw), C. aestivalis (eastern mayhaw), and C. rufula (a possible hybrid between C. opaca and C. aestivalis ) . A 6-component blend was developed for C. opaca (3-methylbutan-1-ol [44%], pentyl acetate [6%], butyl butanoate [6%], propyl hexanoate [6%], butyl hexanoate [26%], and hexyl butanoate [12%]); an 8-component blend for C. aestivalis (3-methylbutan-1-ol [2%], butyl acetate [47%], pentyl acetate [2%], butyl butanoate [12%], propyl hexanoate [1%], butyl hexanoate [25%], hexyl butanoate [9%], and pentyl hexanoate [2%]); and a 9-component blend for C. rufula (3-methylbutan-1-ol [1%], butyl acetate [57%], 3-methylbutyl acetate [3%], butyl butanoate [5%], propyl hexanoate [1%], hexyl propionate [1%], butyl hexanoate [23%], hexyl butanoate [6%], and pentyl hexanoate [3%]). Crataegus aestivalis and C. opaca -origin flies showed significantly higher levels of upwind directed flight to their natal blend in flight tunnel assays compared to the non-natal blend and previously developed apple, northern downy hawthorn, and flowering dogwood blends. Eastern and western mayhaw flies also were tested to the C. rufula blend, with eastern flies displaying higher levels of upwind flight compared with the western flies, likely due to the presence of butyl acetate in the C. aestivalis and C. rufula blends, an agonist compound for eastern mayhaw-origin flies, but a behavioral antagonist for western flies. The results discount the possibility that the apple fly was “pre-assembled” and originated via a recent introduction of southern mayhaw flies predisposed to accepting apple. Instead, the findings are consistent with the possibility of southern mayhaw-infesting fly host races. However, mayhaw fruits do emit several volatiles found in apple. It is, therefore, possible that the ability of the fly to evolve a preference for apple volatiles, although not the entire blend, stemmed, in part, from standing variation related to the presence of these compounds in southern mayhaw fruit.

Phytophagous insects from different feeding guilds may compete indirectly via altering the chemical defenses or nutritional quality of their shared host plants. Gall-formers are understudied in this context but may be susceptible to this mode of competition early in their life history, when they may be particularly sensitive to changes to the specific reactive tissue needed for gall development. Here, we conducted a natural experiment to investigate the effect of folivory of Canada goldenrod, Solidago altissima, by Trirhabda beetles on gall induction success for the goldenrod gall fly, Eurosta solidaginis. We monitored oviposition events and gall development on individual Solidago ramets at sites differing in their levels of Trirhabda folivory. We found a strong inverse relationship between Trirhabda leaf damage and successful gall induction rates. These results suggest Trirhabda beetles may negatively impact Eurosta demographics and highlight the need for further study on how factors affecting gall induction may influence the structure of insect communities.

The apple maggot fly , Rhagoletis pomonella , infests several hawthorn species in the southern USA. In a companion paper, we showed that R. pomonella flies infesting two different mayhaw species ( Crataegus opaca and C. aestivalis ) can discriminate between volatile blends developed for each host fruit, and that these blends are different from previously constructed blends for northern fly populations that infest domestic apple ( Malus domestica ), downy hawthorn ( Crataegus mollis ), and flowering dogwood ( Cornus florida ). Here, we show by using coupled gas chromatography and electroantennographic detection (GC-EAD), gas chromatography with mass spectrometry (GC-MS), and flight tunnel bioassays, that two additional southern hawthorn fly populations infesting C. viridis (green hawthorn) and C. brachyacantha (blueberry hawthorn) also can discriminate between volatile blends for each host fruit type. A 9-component blend was developed for C. viridis (3-methylbutan-1-ol [5%], butyl butanoate [19.5%], propyl hexanoate [1.5%], butyl hexanoate [24%], hexyl butanoate [24%], pentyl hexanoate [2.5%], 1-octen-3-ol [0.5%], pentyl butanoate [2.5%], and (3 E )-4,8-dimethyl-1,3,7-nonatriene (DMNT) [20.5%]) and an 8-component blend for C. brachyacantha (3-methylbutan-1-ol [0.6%], butyl acetate [50%], pentyl acetate [3.5%], butyl butanoate [9%], butyl hexanoate [16.8%], hexyl butanoate [16.8%], 1-octen-3-ol [0.3%], and pentyl butanoate [3%]). Crataegus viridis and C. brachyacantha -origin flies showed significantly higher levels of upwind oriented flight to their natal blend in flight tunnel assays compared to the alternate, non-natal blend and previously developed northern host plant blends. The presence of DMNT in C. viridis and butyl acetate in C. brachyacantha appeared to be largely responsible for driving the differential response. This sharp behavioral distinction underscores the diversity of odor response phenotypes in the southern USA, points to possible host race formation in these populations, and despite the presence of several apple volatiles in both blends, argues against a functional apple race existing on southern host plants prior to the introduction of apple to North America.

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.