Oak gall wasps (Hymenoptera: Cynipidae, Cynipini) are characterized by possession of complex cyclically parthenogenetic life cycles and the ability to induce a wide diversity of highly complex species- and generation-specific galls on oaks and other Fagaceae. The galls support species-rich, closed communities of inquilines and parasitoids that have become a model system in community ecology. We review recent advances in the ecology of oak cynipids, with particular emphasis on life cycle characteristics and the dynamics of the interactions between host plants, gall wasps, and natural enemies. We assess the importance of gall traits in structuring oak cynipid communities and summarize the evidence for bottom-up and top-down effects across trophic levels. We identify major unanswered questions and suggest approaches for the future.
How geographically widespread biological communities assemble remains a major question in ecology. Do parallel population histories allow sustained interactions (such as host-parasite or plant-pollinator) among species, or do discordant histories necessarily interrupt them? Though few empirical data exist, these issues are central to our understanding of multispecies evolutionary dynamics. Here we use hierarchical approximate Bayesian analysis of DNA sequence data for 12 herbivores and 19 parasitoids to reconstruct the assembly of an insect community spanning the Western Palearctic and assess the support for alternative host tracking and ecological sorting hypotheses. We show that assembly occurred primarily by delayed host tracking from a shared eastern origin. Herbivores escaped their enemies for millennia before parasitoid pursuit restored initial associations, with generalist parasitoids no better able to track their hosts than specialists. In contrast, ecological sorting played only a minor role. Substantial turnover in host-parasitoid associations means that coevolution must have been diffuse, probably contributing to the parasitoid generalism seen in this and similar systems. Reintegration of parasitoids after host escape shows these communities to have been unsaturated throughout their history, arguing against major roles for parasitoid niche evolution or competition during community assembly.
A quantitative catalogue of the parasitoids (almost exclusively Chalcidoidea) and inquiline Cynipidae recorded in the western Palaearctic from galls induced on Quercus by Cynipidae (Cynipini) is presented. Quantitative and national data are included with bibliographic references to almost all records published in 2011 and earlier. The catalogue is followed by two checklists, firstly one of the Chalcidoidea with numbers of each species recorded from each type of host gall (galls of the sexual and asexual generations of the host gall wasps are listed separately), and secondly one of inquiline Cynipidae with host galls. Compared to non-oak gall wasps, the Cynipini support a much larger parasitoid and especially inquiline fauna, and this fauna is very largely restricted at the species level to Cynipini galls. About one hundred chalcidoid species are recorded from galls of Cynipini, distributed over six families: Pteromalidae and Eulophidae (29 species each), Torymi-dae (21 species), Eurytomidae (10 species), Eupelmidae (8 species) and Ormyridae (at least 2 species). Polyphagy is usual in the chalcidoid parasitoids, most species having a broad host gall range, but quantitatively the fauna of each type of oak gall is rather characteristic and is strongly influenced by gall morphology, situation on the tree, season of growth and host tree species. These and other extrinsic factors restrict the full exploitation of the chalcidoids’ potential host gall range.
Large morphological phylogenetics analyses are often poorly documented because of the constraints of traditional print journals, making it difficult to critically evaluate the data and build on it in future studies. We use modern information technology to overcome this problem in a comprehensive analysis of higher relationships among oak gall wasps and their closest relatives. Our morphological characters are documented by more than 2,000 images deposited in the open web image database Morphbank (http://www.morphbank.net), allowing one-click access from character and character state descriptions to the raw data. The oak gall wasps (Cynipidae: Cynipini) form one of the largest specialized radiations of galling insects with almost 1,000 described species attacking oaks or oak relatives. According to previous morphological studies, the Cynipini form a monophyletic clade, the Woody Rosid Gallers (WRG), together with three small cynipid tribes (Diplolepidini, Eschatocerini, and Pediaspidini). The WRG all attack woody representatives of the rosid clade of eudicots. Little was previously known about higher WRG relationships. We studied 54 exemplar taxa of WRG, including representatives from 34 of the 41 valid genera of oak gall wasps, and two outgroups. The study resulted in 308 characters, 283 from morphology and 25 from biology and distribution; most of these are original to the present paper. Parsimony analyses supported the monophyly of three major WRG lineages: Diplolepidini + Eschatocerini, Pediaspidini + Paraulax, and Cynipini. The poorly known South American genus Paraulax, developing in galls on Nothofagus, is moved from Cynipini to Pediaspidini to reflect these results. The single Japanese species described in Paraulax by Shinji (types lost) is transferred to Ceroptres as C. quereicola (Shinji 1938) comb. nov. Two major lineages of oak gallers were recognized in most analyses: (1) the Neuroterus-group (Neuroterus, Pseudoneuroterus, the previously recognized genus Trichagalma, Plagiotrochus, possibly also Palearctic Dryocosmus and Aphelonyx+Disholcaspis); and (2)the Cynips-group (Cynips, Belonocnema, Atrusca, Acraspis, Philonix, Biorhiza and Trigonaspis). The large and problematic genus Andricus was paraphyletic in some analyses and monophyletic in others, with Disholcaspis spectabilis being the sister to other Cynipini in the former case and European Callirhytis in the latter. Our results suggest that WRG are conservative in their host plant preferences but there is no evidence for parallel insect-plant cladogenesis. Distributional patterns suggest a possible origin for the oak gall wasps in the Nearctic but the picture is otherwise complicated. Both heterogeny, the cyclical alternation of sexual and parthenogenetic generations, and heteroecy, the use of different sections of Quercus as host for the two generations, appear to have evolved twice within the WRG.
The invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) causes serious economic damage in several soft fruit crops. This study aimed (1) to identify naturally occurring parasitoids and predators of this pest in North East Spain and (2) to get preliminary data on their potential as pest biological control agents. Two parasitoid species were found spontaneously parasitizing D. suzukii: Pachycrepoideus vindemmiae (Rondani) (Hymenoptera: Pteromalidae) and Trichopria cf. drosophilae Perkins (Hymenoptera: Diapriidae). Both species were found repeatedly through the survey period and successfully reproduced in the laboratory on D. suzukii pupae. In addition, both species strongly reduced adult emergence of D. suzukii from infested fruits. Regarding predators, Orius laevigatus (Fieber) (Hemiptera: Antochoridae) were able to feed on D. suzukii eggs but not on larvae whereas the soil predator Labidura riparia Pallas (Dermaptera: Labiduridae) consumed D. suzukii larvae and pupae and was effective in reducing pest populations in laboratory tests.
The Eucoilinae are a diverse and important group of relationships among these three lineages. Of the 6 eucoiline genus groups recognized by Nordlander in 1982 parasitoids of Diptera, particularly in the tropics, but (Entomol. Scand. 13, 269-292), only 2 are supported as they are poorly known systematically and their generic monophyletic: the Trybliographa and Kleidotoma groups. classification is partly chaotic. Here, we present the first The Gronotoma group is a paraphyletic assemblage of comprehensive cladistic analysis of higher eucoiline relatwo different basal clades of eucoilines. The Rhoptromeris tionships. The analysis is based on 148 skeletal characgroup is unnatural and only the 2 core genera, Rhoptromters of adults documented in more than 1100 digital eris and Trichoplasta, form a monophyletic lineage. The images available in an Internet-accessible database. The data are ambiguous concerning the Ganaspis group, characters were coded for 45 taxa representing 35 eucoiwhich appears to be paraphyletic, and the Chrestosema line genera, spanning the entire diversity of the group, group, which may be a good clade. Based on the results and 7 outgroup genera. Relationships were partly diffiwe propose a modified system of informal genus groups cult to resolve and parsimony analysis under implied in the Eucoilinae and discuss putative synapomorphies weights performed considerably better than analysis supporting each genus group. The proposed relationunder uniform weights. The results support the monoships imply that the first eucoilines were parasitoids of phyly of the Eucoilinae and show that eucoilines are most leaf-mining agromyzids. The earliest split in the group closely related to the figitid subfamilies Emargininae and was apparently between an Afrotropical and a NeotropiPycnostigminae, but are ambiguous concerning the exact cal lineage, and much of the early radiation of the group occurred in these regions, particularly in the Neotropics. ᭧
Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.
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