Oak Gall Wasps Research Articles

Current and Future Insect Threats to Oaks of the Midwest, Great Lakes, and Northeastern United States and Canada

Increasing temperatures, prolonged drought, the increased severity and intensity of storms, and other effects of climate change are being felt globally, and long-lived forest tree species may struggle in their current ranges. Oaks (Quercus spp.) have evolved a range of adaptations to dry and hot conditions and are believed to be a “climate change winner” by increasing their suitable habitat. However, a mixture of life history traits and increasing susceptibility to herbivores and xylovores as well as secondary pathogen infections still put oaks at risk of decline. Oak species found in the Midwestern, Great Lakes, and Northeastern United States and Canada are important keystone species with high ecological and economical importance. They are also vulnerable to existing, new, and emerging threats that have the potential to cause mortality across entire stands quickly. Current examples of insect threats include the Lymantria dispar (spongy moth), Agrilus bilineatus (twolined chestnut borer), and Nitidulidae (sap beetles) as disease vectors. Examples of emerging insects of concern include Cynipidae (oak gall wasps) and Enaphalodes rufulus (red oak borer). This study describes these insects, explains their mechanisms of action and the effects on oaks, and explores mitigation strategies for each.

Reticulodermis lithogalla gen. nov. and sp. nov. of oak gall wasp from Mexico (Hymenoptera, Cynipidae)

A new genus of oak gall wasp, Reticulodermis Pujade-Villar, Cuesta-Porta & Melika gen. nov. and a new species R. lithogalla García-Martiñón & Pujade-Villar sp. nov. are described from Mexico. Reticulodermis is known only from the asexual generation that induces galls on leaves of Quercus crassipes Humb. & Bonpl. (section Lobatae). We provide the diagnosis, distribution and biological data on the new species. An identification key to the genera of oak gall wasps inducing galls on the section Lobatae is given.

Modelling suggests Wolbachia-induced cytoplasmic incompatibility in oak gall wasps with cyclical parthenogenesis.

Oak gall wasps typically exhibit a life cycle with one sexual and one asexual generation each year. These wasps can carry various endosymbionts, one of which is the maternally inherited bacterium Wolbachia that can induce several reproductive manipulations on its host. Cytoplasmic incompatibility (CI) has been described as the most prominent of these manipulations. CI leads to embryonic mortality in the hosts' offspring when infected males mate with either uninfected females or with females that harbour different Wolbachia strains. It has been hypothesized that Wolbachia can induce CI in oak gall wasps. To address this hypothesis, we derived a mathematical model to investigate the spread of a bacterial infection in naive populations and to determine the plausibility of CI occurrence. To validate our model, we used published data from Wolbachia-infected Belonocnema kinseyi populations in two approaches. Our first approach uses measurements of infection frequencies and maternal transmission in the sexual generation. For the second approach, we extended the model to compare predictions to estimates of mtDNA-haplotypes, which, like Wolbachia, are maternally inherited, and can therefore be associated with the infection. Both approaches indicate that CI is present in these populations. Our model can be generalized to investigate the occurrence of CI not only for oak gall wasps but also for other species.

Comparative transcriptome reprogramming in oak galls containing asexual or sexual generations of gall wasps.

Oak gall wasps have evolved strategies to manipulate the developmental pathways of their host to induce gall formation. This provides shelter and nutrients for the developing larva. Galls are entirely host tissue; however, the initiation, development, and physical appearance are controlled by the inducer. The underlying molecular mechanisms of gall formation, by which one or a small number of cells are reprogrammed and commit to a novel developmental path, are poorly understood. In this study, we sought a deeper insight into the molecular underpinnings of this process. Oak gall wasps have two generations each year, one sexual, and one asexual. Galls formed by these two generations exhibit a markedly different appearance. We sequenced transcriptomes of both the asexual and sexual generations of Neuroterus quercusbaccarum and Neuroterus numismalis. We then deployed Nanopore sequencing to generate long-read sequences to test the hypothesis that gall wasps introduce DNA insertions to determine gall development. We detected potential genome rearrangements but did not uncover any non-host DNA insertions. Transcriptome analysis revealed that transcriptomes of the sexual generations of distinct species of wasp are more similar than inter-generational comparisons from the same species of wasp. Our results highlight the intricate interplay between the host leaves and gall development, suggesting that season and requirements of the gall structure play a larger role than species in controlling gall development and structure.

Description of the first species of gall wasp (Hym., Cynipidae: Cynipini) on Quercus grahamii (Fagaceae).

A new species of oak gall wasp, Andricus coombesi Pujade-Villar & Prez-Torres n. sp. from Mexico, known only from its asexual generation that induces galls on acorns of Quercus grahamii Benth., (section Lobatae) is described. Its presence causes the complete disappearance of the acorn. Diagnosis, distribution and biological data of the new species are given. Andricus coombesi Pujade-Villar & Prez-Torres n. sp. represents the first gall wasp species mentioned from this host.

Speciation in kleptoparasites of oak gall wasps often correlates with shifts into new tree habitats, tree organs, or gall morphospace.

Host shifts to new plant species can drive speciation for plant-feeding insects, but how commonly do host shifts also drive diversification for the parasites of those same insects? Oak gall wasps induce galls on oak trees and shifts to novel tree hosts and new tree organs have been implicated as drivers of oak gall wasp speciation. Gall wasps are themselves attacked by many insect parasites, which must find their hosts on the correct tree species and organ, but also must navigate the morphologically variable galls with which they interact. Thus, we ask whether host shifts to new trees, organs, or gall morphologies correlate with gall parasite diversification. We delimit species and infer phylogenies for two genera of gall kleptoparasites, Synergus and Ceroptres, reared from a variety of North American oak galls. We find that most species were reared from galls induced by just one gall wasp species, and no parasite species was reared from galls of more than four species. Most kleptoparasite divergence events correlate with shifts to non-ancestral galls. These shifts often involved changes in tree habitat, gall location, and gall morphology. Host shifts are thus implicated in driving diversification for both oak gall wasps and their kleptoparasitic associates.

Phylogenomic analysis of protein‐coding genes resolves complex gall wasp relationships

AbstractGall wasps (Hymenoptera: Cynipidae) comprise 13 distinct tribes whose interrelationships remain incompletely understood. Recent analyses of ultra‐conserved elements (UCEs) represent the first attempt at resolving these relationships using phylogenomics. Here, we present the first analysis based on protein‐coding sequences from genome and transcriptome assemblies. Unlike UCEs, these data allow more sophisticated substitution models, which can potentially resolve issues with long‐branch attraction. We include data for 37 cynipoid species, including two tribes missing in the UCE analysis: Aylacini (s. str.) and Qwaqwaiini. Our results confirm the UCE result that Cynipidae are not monophyletic. Specifically, the Paraulacini and Diplolepidini + Pediaspidini fall outside a core clade (Cynipidae s. str.), which is more closely related to the insect‐parasitic Figitidae, and this result is robust to the exclusion of long‐branch taxa that could mislead the analysis. Given this, we here divide the Cynipidae into three families: the Paraulacidae stat. prom., Diplolepididae stat. prom. and Cynipidae (s. str.). Our results suggest that the Eschatocerini are the sister group of the remaining Cynipidae (s. str.). Within the Cynipidae (s. str.), the Aylacini (s. str.) are more closely related to oak gall wasps (Cynipini) and some of their inquilines (Ceroptresini) than to other herb gallers (Aulacideini and Phanacidini), and the Qwaqwaiini likely form a clade together with Synergini (s. str.) and Rhoophilini. Several alternative scenarios for the evolution of cynipid life histories are compatible with the relationships suggested by our analysis, but all are complex and require multiple shifts among parasitoids, inquilines and gall inducers.

Host–enemy interactions provide limited biotic resistance for a range‐expanding species via reduced apparent competition

AbstractAimAs species' ranges shift poleward in response to anthropogenic change, they may lose antagonistic interactions if they move into less diverse communities, fail to interact with novel populations or species effectively, or if ancestral interacting populations or species fail to shift synchronously. We leveraged a poleward range expansion in a tractable insect host–enemy community to uncover mechanisms by which altered antagonistic interactions between native and recipient communities contributed to ‘high niche opportunities’ (limited biotic resistance) for a range‐expanding insect.LocationNorth America, Pacific Northwest.MethodsWe created quantitative insect host–enemy interaction networks by sampling oak gall wasps on 400 trees of a dominant oak species in the native and expanded range of a range‐expanding gall wasp species. We compared host–enemy network structure between regions. We measured traits (phenology, morphology) of galls and interacting parasitoids, predicting greater trait divergence in the expanded range. We measured function relating to host control and explored if altered interactions and traits contributed to reduced function, or biotic resistance.ResultsInteraction networks had fewer species in the expanded range and lower complementarity of parasitoid assemblages among host species. While networks were more generalized, interactions with the range‐expanding species were more specialized in the expanded range. Specialist enemies effectively tracked the range‐expanding host, and there was reduced apparent competition with co‐occurring hosts by shared generalist enemies. Phenological divergence of enemy assemblages interacting with the range‐expanding and co‐occurring hosts was greater in the expanded range, potentially contributing to weak apparent competition. Biotic resistance was lower in the expanded range, where fewer parasitoids emerged from galls of the range‐expanding host.Main ConclusionsChanges in interactions with generalist enemies created high niche opportunities, and limited biotic resistance, suggesting weak apparent competition may be a mechanism of enemy release for range‐expanding insects embedded within generalist enemy networks.

The role of Anatolia between Asia and Europe: A case study of oak gall wasp species, Cynips quercus (Hymenoptera, Cynipidae)

In this study, we used DNA sequence data of a western Palearctic oak gall wasp species, Cynips quercus, showing distribution from Europe to Iran to answer the following questions: i) Do the eastern C. quercus populations have higher genetic diversity than the European populations?, ii) Are the eastern populations source for the European populations?, iii) What is the possible date of divergence between the Asian and European populations? For these purposes, we analysed 88 cytochrome b sequences representing Iran, Türkiye, Hungary, and Spain. Our analyses revealed that the highest genetic diversity was in Türkiye followed by Iran, Hungary, and Spain, respectively. Iranian samples were most divergent from the Spain and Hungary sequences. Pairwise comparisons showed that the highest gene flow was between Türkiye and Hungary, and between Türkiye and Iran, respectively. Phylogenetic analysis grouped the Turkish haplotypes with the Iranian sequences, and Spain was grouped with Hungary. Network analysis revealed that the western Turkish samples were separated from eastern sequences, and all of the eastern Turkish sequences were clustered with the Iranian samples meanwhile a western Turkish lineage provided a source to Hungary and then to Spain. Times of divergence analysis estimated that the Turkish lineage split from the Iranian lineage around 4,67 million years ago, and Hungarian and Spanish lineages diverged from each other about 3 million years ago. Correspondingly, our analyses suggested that Anatolia played a key role as a bridge between the Asian and European populations of C. quercus.

Plant Gall Diversity in Burned Semi-natural Grasslands in Japan

We surveyed woody plants, including oaks and chestnuts (Quercus L. and Castanea Mill.), and recorded the inhabiting galls induced by oak gall wasps (Hymenoptera: Cynipidae: Cynipini) at seven Japanese semi-natural grassland sites maintained by traditional regular burning with two of the seven abandoned grassland areas. Woody plants were established in all burned and abandoned grasslands. Oak species were found at four of the seven sites. In total, 15 types of cynipid galls were recorded at all four sites where oak species were found. However, the occurrence of species was site-specific for host trees and cynipid galls. Although a few ecological studies of oak gall wasps inhabiting grassland environments, which have rapidly decreased in recent decades, have been conducted, this study suggests that semi-natural grasslands may be potential habitats for oak gall wasps and their host trees, and we provide a checklist of oak gall wasps with host oak records in semi-natural grasslands throughout Japan.

Dependence of the species diversity of oak gall wasps on the physiological heterogeneity of Quercus robur

Dependence of the species diversity of oak gall wasps on the physiological heterogeneity of Quercus robur

Latitudinal gradient in species diversity provides high niche opportunities for a range-expanding phytophagous insect.

When species undergo poleward range expansions in response to anthropogenic change, they likely encounter less diverse communities in new locations. If low diversity communities provide weak biotic interactions, such as reduced competition or predation, range-expanding species may experience high niche opportunities. Here, we investigated if oak gall wasp communities follow a latitudinal diversity gradient (LDG) and if lower diversity communities provide weaker interactions at the poles for a range-expanding community member, Neuroterus saltatorius. We performed systematic surveys of gall wasps on a dominant oak, Quercus garryana, throughout most of its range, from northern California to Vancouver Island, British Columbia. On 540 trees at 18 sites, we identified 23 oak gall wasp morphotypes in three guilds (leaf detachable, leaf integral, and stem galls). We performed regressions between oak gall wasp diversity, latitude, and other abiotic (e.g. temperature) and habitat (e.g. oak patch size) factors to reveal if gall wasp communities followed an LDG. To uncover patterns in local interactions, we first performed partial correlations of gall wasp morphotype occurrences on trees within regions). We then performed regressions between abundances of co-occurring gall wasps on trees to reveal if interactions are putatively competitive or antagonistic. Q. garryana-gall wasp communities followed an LDG, with lower diversity at higher latitudes, particularly with a loss of detachable leaf gall morphotypes. Detachable leaf gall wasps, including the range-expanding species, co-occurred most on trees, with weak co-occurrences on trees in the northern expanded region. Abundances of N. saltatorius and detachable and integral leaf galls co-occurring on trees were negatively related, suggesting antagonistic interactions. Overall, we found that LDGs create communities with weaker associations at the poles that might facilitate ecological release in a range-expanding community member. Given the ubiquity of LDGs in nature, poleward range-expanding species are likely moving into low diversity communities. Yet, understanding if latitudinal diversitypattern provides weak biotic interactions for range-expanding species is not well explored. Our large-scale study documenting diversity in a related community of phytophagous insects that co-occur on a host plant reveals that LDGs create high niche opportunities for a range-expanding community member. Biogeographical patterns in diversity and species interactions are likely important mechanisms contributing to altered biotic interactions under range-expansions.

Andricus protuberans Pujade-Villar & Ferrer-Suay IS A SEXUAL FORM (HYM., CYNIPIDAE, CYNIPINI)

We describe and illustrate the morphological characters of the male of Andricus protuberans Pujade-Villar & Ferrer-Suay, 2015 (Hymenoptera, Cynipidae), an oak gall wasp species considered an asexual generation in the original description. The reasons for this mistake are discussed, and the variability of this species in the metasomal segments is mentioned.

Discovery through iNaturalist: new species and new records of oak gall wasps (Hymenoptera: Cynipidae: Cynipini) from Texas, USA.

A new species of the genus Druon Kinsey, 1937, D. laceyi Zhang, Sasan OKennon sp. nov. is described on host plant Quercus laceyi Small from central Texas. We also re-establish Andricus lustrans Beutenmller, 1913 comb.rev., and transfer Striatoandricus aciculatus (Beutenmller, 1909) comb. nov. from Andricus. Finally, we report a new state and host record for Druon gregori Melika, Nicholls Stone, 2022. All observations were first shared on the social platform iNaturalist, highlighting the potential of cybertaxonomy in uncovering overlooked biodiversity.

Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both.

Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae—primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host‐associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host‐associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants.

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data.

Cryptic species diversity is a major challenge regarding the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the USA, we combined mitochondrial DNA barcodes, ultraconserved elements (UCEs), morphological and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.

A catalogue, revision, and regional perspective of Eastern Palaearctic and Oriental oak gall wasps and their inquilines (Hymenoptera: Cynipidae: Cynipini, Synergini, Ceroptresini).

Recent years have seen rapid advances in the study of Fagaceae-associated gall wasps (Hymenoptera: Cynipidae) of the Eastern Palaearctic and the Oriental (EPO) regions, for both the gall inducing Cynipini (commonly termed oak gall wasps though many species gall non-oak Fagaceae) and the predominantly inquiline tribes Synergini and Ceroptresini. This process has propagated some taxonomic errors and involves many taxa whose taxonomic status is uncertain. To provide a stable foundation for further advance, here we review the taxonomic status of the 212 species (133 oak gall wasps and 79 oak cynipid inquilines) that have been described or recorded in these regions. Of this total, we treat 171 as valid species names (103 oak gall wasps and 68 oak cynipid inquilines) in 20 genera; 22 as synonym names, 13 as incertae sedis, three as nomen dubium, and three as species inquirenda. Callirhytis kunugicola Shinji, 1944 is proposed as syn. nov. of C. kunugicola Shinji, 1943, as Shinji described the same species twice. For all valid species names, we provide taxonomic references, synonyms, and geographical distributions. We summarize what is known of host plant associations and gall locations for gall inducers, and host associations for inquilines. We discuss geographic patterns in the known richness of currently valid species for both groups of organisms, and place this in the context of the biogeography of available Fagaceae host plants. We provide a brief historical review of the study of oak gall wasps and their inquilines in the EPO regions.

Pairing of sexual and asexual generations of Nearctic oak gallwasps, with new synonyms and new species names (Hymenoptera: Cynipidae, Cynipini).

Most oak gallwasps (Hymenoptera; Cynipidae, Cynipini) have lifecycles involving obligate alternation between a sexual and an asexual generation. Many species are currently known from only one of these generations, with the alternate generation either unknown or separately described with a different name. Here we describe previously unknown generations for 12 Nearctic oak cynipids. We describe the sexual generation for ten species previously known only from an asexual generation: Acraspis quercushirta (Bassett, 1864), Acraspis villosa Gillette, 1888, Amphibolips spinosa Ashmead, 1887, Andricus balanaspis (Weld, 1922), comb. nov., Antron quercusnubila (Bassett, 1881), Bassettia pallida Ashmead, 1896, Neuroterus floccosus (Bassett, 1881), comb. rev., Philonix fulvicollis Fitch, 1859, Phylloteras poculum (Osten Sacken, 1862) and Sphaeroteras carolina (Ashmead, 1887), comb. rev.. We describe the asexual generation of Bassettia flavipes (Gillette, 1889), comb. nov. and Melikaiella tumifica (Osten Sacken, 1865), both previously known only from a sexual generation. Three described taxa (Neuroterus vernus Gillette, 1889, syn. nov., Neuroterus papillosus Beutenmueller, 1910, syn. nov. and Neuroterus perminimus Bassett, 1900, syn. nov.) are all identified as the sexual generation of Neuroterus niger Gillette, 1888. We also comment on the presence of previously unknown non-functional males reared from galls of the asexual generation of Neuroterus niger. We identify two further synonyms: Acraspis macrocarpae Bassett, 1890 is syn. nov. of A. quercushirta (Bassett, 1864), and Bassettia archboldi Melika Abrahamson, 2007 is syn. nov. of Bassettia pallida Ashmead, 1896. In addition, we formally synonymise multiple varieties described by Kinsey within his Acraspis quercushirta, A. villosa, Antron quercusnubila, Neuroterus niger and Philonix fulvicollis species complexes. We provide descriptions and diagnoses for these taxa, and summarise what is known of their biology, including host associations. All taxa and relationships between alternate generations are supported by morphological and molecular data.

Re-establishment of the Nearctic oak cynipid gall wasp genus Druon Kinsey, 1937 (Hymenoptera: Cynipidae: Cynipini), with description of five new species.

The Nearctic cynipid oak gall wasp genus Druon Kinsey comb. rev. is re-established, with 5 new species and 10 species previously placed in the genus Andricus Hartig 1840: D. alexandri Melika, Nicholls Stone, sp. nov., D. flocculentum (Lyon), comb. nov., D. fullawayi (Beutenmller), comb. nov., D. garciamartinonae Pujade-Villar, sp. nov., D. gregori Melika, Nicholls Stone, sp. nov., D. hansoni Cuesta-Porta, Melika Pujade-Villar, sp. nov., D. ignotum (Bassett), comb. nov., D. linaria Kinsey, comb. rev., D. pattoni (Bassett), comb. nov., D. protagion Kinsey, comb. rev. (D. malinum Kinsey, syn. nov., D. polymorphae Kinsey, syn. nov.), D. quercusflocci (Walsh), comb. nov., D. quercuslanigerum (Ashmead), comb. nov., D. receptum Kinsey, comb. rev., D. rusticum Kinsey, comb. rev. and D. serretae Pujade-Villar, Cuesta-Porta Melika, sp. nov.. All species are known only from their asexual generation except for D. ignotum and D. quercuslanigerum, for which alternating asexual and sexual generations are known. The sexual generation of D. ignotum and a new morphological variety of D. quercuslanigerum from Mexico are both described for the first time. We provide descriptions, redescriptions, diagnoses, keys to species, DNA sequence data and analyses, and information on biology, phenology, and distribution. Additionally, four Andricus species with woolly galls and striato-reticulated metasomas are transferred to Striatoandricus Pujade-Villar: S. furnessulus, comb. nov., S. furnessae, comb. nov., S. guatemalensis, comb. nov., and S. tenuicornis, comb. nov.

A new species of oak gall wasp (Hymenoptera: Cynipidae, Cynipini) from Turkey.

A new species of the genus Andricus Hartig, 1840 (Cynipidae: Cynipini) is described from Burdur province in Turkey: Andricus arslani Azmaz Katlm sp. n. sexual generation. The new species induce galls on Quercus cerris L. belonging to section Cerris. SEM images, photos of the host galls, and data on the diagnosis, distribution, and biology of the new species are provided.