Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp.

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.

Flagellar Sensillar Equipment of Two Morphologically Closely Related Aphid Hyperparasitoids (Hymenoptera: Figitidae: Alloxysta).

The antennal sensillar equipment in the parasitic wasp family Figitidae was analyzed to date only in few species, despite some are associated with crop pests and can have an economic importance. It is the case of the genus Alloxysta, which includes hyperparasitoids of aphids which can potentially reduce effectiveness of primary pest parasitoids. Here we analyzed, through scanning electron microscopy, the diversity, morphology, and distribution of the antennal sensilla in males and females of Alloxysta consobrina (Zetterstedt) and Alloxysta victrix (Westwood), two species with overall very similar morphology. In both species, antennae are filiform and cylindrical, and flagellum was longer in A. victrix. Eight sensillar types have been recognized: four types of sensilla trichoidea (ST-A, ST-B, ST-C, ST-D), sensilla coeloconica, sensilla placoidea, sensilla campaniformia, and sensilla basiconica. ST-A, ST-B, ST-C, and sensilla placoidea were the most abundant types on the antennae and often increased in number and decreased in size toward the tip of antenna. The two species seem to have several differences in their sensillar equipment, possibly in accordance with the different degree of host range. On the other hand, sexual dimorphism is probably due to the different stimuli that have to be correctly processed. The comparison with the other species of Figitidae studied by far showed, at subfamily-level, that variability in sensillar equipment and phylogeny do not agree. This suggests a complex series of morphological changes during evolution of this group. The taxonomic sample should be thus substantially enlarged to disclose possible trends in sensillar equipment evolution in the family.

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.

Description of a new genus and species of Eucoilinae (Hymenoptera: Cynipoidea: Figitidae) from Colombia.

Fontaliella, a new genus of Eucoilinae (Hymenoptera, Cynipoidea, Figitidae) and E. colombiensis sp. nov. from Colombia, are described and illustrated. This new genus belongs to the Ganaspini and morphologically resembles Zamischus Ashmead, 1903, Perischus Weld, 1931 and Steleucoela Kieffer, 1908. A key to differentiate these genera and species is given.

Revision of Apocharips Fergusson (Hymenoptera: Figitidae: Charipinae) with description of three new species from Colombia.

The genus Apocharips is here revised. Three previously described species are considered as valid: Apocharips angelicae Pujade-Villar & Evenhuis, 2002, A. hansoni Menke, 1993, and A. trapezoidea (Hartig, 1841). Apocharips eleaphila (Silvestri, 1915) and A. peraperta (Silvestri, 1915) are synonymyzed with A. trapezoidea. Three new species are here described: Apocharips colombiana Ferrer-Suay & Pujade-Villar n. sp., Apocharips tamanii Paretas-Martinez & Pujade-Villar n. sp. and Apocharips tropicale Ferrer-Suay & Paretas-Martinez n. sp. A key to the six species included in Apocharips is given.

Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic.

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.

Overview of the current status of Charipinae (Hymenoptera, Cynipoidea, Figitidae): taxonomy, distribution, and diversity.

The subfamily Charipinae (Hymenoptera: Cynipoidea: Figitidae) has had a problematic taxonomic history as many species have been described without comprehensive revisions being undertaken. Reliably identifying these species based on morphological assessment has been almost impossible. Recently, the types of all species have been re-examined and photographed, resulting in numerous taxonomic corrections that have been published elsewhere. Consequently, a summary checklist of all species that have ever been described within the Charipinae is provided with their current accepted status, including all associated references dealing with the historical nomenclatural changes and synonymy. We also provide up-to-date information on the diversity and distribution patterns of Charipinae to assist researchers working on these species in aphid biological control programs.

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

The Nearctic cynipid oak gall wasp genus Feron Kinsey, comb. rev., is re-established with 34 species: F. albicomus (Weld, 1952), comb. nov., F. amphorus (Weld, 1926), comb. nov., F. apiarium (Weld, 1944), comb. nov., F. atrimentum (Kinsey, 1922), comb. nov., F. bakkeri (Lyon, 1984), comb. nov., F. caepula (Weld, 1926), comb. nov., F. californicum (Beutenmueller, 1911), comb. nov., F. clarkei (Bassett, 1890), comb. nov., F. comatum (Weld, 1952), comb. nov., F. crystallinum (Bassett, 1900), comb. nov., F. cylindratum (Kinsey, 1937), comb. nov., F. discale (Weld, 1926), comb. nov., F. discularis (Weld, 1926), comb. nov., F. dumosae (Weld, 1957), comb. nov., F. gigas (Kinsey, 1922), comb. nov., F. izabellae Melika, Nicholls & Stone, sp. nov., F. kingi (Bassett, 1900), comb. nov., F. parmula (Bassett, 1900), comb. nov., F. pattersonae (Fullaway, 1911), comb. nov., F. roberti Melika, Nicholls & Stone, sp. nov., F. rucklei Melika, Nicholls & Stone, sp. nov., F. scutellum (Weld, 1930), comb. nov., F. serranoae Pujade-Villar & Cuesta-Porta, sp. nov., F. splendens (Weld, 1919), comb. nov., F. stellare (Weld, 1926), comb. nov., F. stellulum (Burnett, 1974), comb. nov., F. sulfureum (Weld, 1926), comb. nov., F. syndicorum Pujade-Villar & Cuesta-Porta, sp. nov., F. tecturnarum (Kinsey, 1920), comb. nov., F. tetyanae Melika, sp. nov., F. tibiale Kinsey, 1937, comb. rev., F. tubifaciens (Weld, 1926), comb. nov., F. verutum Kinsey, 1937, comb. rev., and F. vitreum Kinsey, 1937, comb. rev. Most species are known only from the asexual generation; F. clarkei, F. comatum, and F. dumosae are known only from the sexual generation, while both generations are recognised for F. atrimentum, F. crystallinum, F. gigas, F. kingi, and F. pattersonae. Matching of alternate sexual and asexual generations is established for the first time for F. kingi and F. pattersonae (= Andricus pedicellatus (Kinsey, 1922), syn. nov.) based on molecular data (both cytb and ITS2 sequences). Morphological descriptions, re-descriptions, diagnoses, and a key to species are given, as well as data on DNA sequences, biology, phenology, and distribution.

Revision of the Amphibolips niger group with the description of a new species (Hymenoptera: Cynipini).

Amphibolips is currently divided into two species-groups, clearly differentiated by adult and gall morphology. The niger group of Amphibolips species is revised. This complex includes eight species: A. gumia Kinsey, A. jubatus Kinsey, A. elatus Kinsey, A. maturus Kinsey, A. nebris Kinsey, A. niger Kinsey, A. pistrix Kinsey and A. ufo Cuesta-Porta & Pujade-Villar sp. nov. We provide descriptions of new species and re-descriptions of known species, diagnoses, keys to complexes and species. The possibility of the niger complex belonging to a new genus is also discussed.

Description of the first brachypterous Lonchidia species (Hymenoptera: Figitidae: Figitinae), with a key to European species.

The male and female of a new species of Lonchidia Thomson, 1862, L. atypica Pujade-Villar & de Paz sp. nov., are described from the provinces of Salamanca and Cceres (Western Spain). Specimens were collected with a G-Vac suction sampler and pitfall traps from traditional almond and cherry orchards. The diagnostic characters of this species are: deep but short notauli, reaching only the anterior part of the mesoscutum, and brachypterous wings. Both sexes are illustrated and an identification key is proposed herein to differentiate the European species. The possibility that the male of L. clavicornis Thomson, 1862 corresponds to a different species is also discussed.

New herb gall wasps from Iran (Hymenoptera: Cynipidae).

Five new gall wasp species, Aulacidea koeiana Melika, Tavakoli Stone, sp. nov., A. lorestanica Melika, Tavakoli Stone, sp. nov., A. piroziae Melika, Stone Pujade-Villar, sp. nov., Phanacis strigosa Melika, Stone Tavakoli, sp. nov., P. tavakolii Melika, Stone Pujade-Villar, sp. nov. are described from Lorestan, Iran. Descriptions, diagnoses, plus information on biology and host associations are given for all new species, and we provide the first description of the male of Isocolus beheni Melika Karimpour, 2008.

A new species of the inquilinous gall wasp genus Saphonecrus Dalla-Torre & Kieffer (Hymenoptera: Cynipidae: Synergini) from South Korea, Saphonecrus jejuensis Kang & Lobato-Vila, sp. nov.

A new species of the inquilinous gall wasp genus Saphonecrus (Hymenoptera: Cynipidae: Synergini) reared from undetermined cryptic stem galls on Quercus glauca Thunb., Saphonecrus jejuensis Kang & Lobato-Vila, sp. nov., is described from South Korea. A detailed description, diagnosis, data on biology and pictures of both the new species and the host galls are provided. An identification key to the Saphonecrus species found in South Korea is also given.

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 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.

Taxonomic and functional responses to fire and post-fire management of a Mediterranean hymenoptera community.

Fire is one of the commonest disturbances worldwide, transforming habitat structure and affecting ecosystem functioning. Understanding how species respond to such environmental disturbances is a major conservation goal that should be monitored using functionally and taxonomically diverse groups such as Hymenoptera. In this respect, we have analyzed the taxonomic and functional response to fire and post-fire management of a Hymenoptera community from a Mediterranean protected area. Thus, Hymenoptera were sampled at fifteen sites located in three burnt areas submitted to different post-fire practices, as well as at five sites located in peripheral unburnt pine forest. A total of 4882 specimens belonging to 33 families, which were classified into six feeding groups according to their dietary preferences, were collected. ANOVA and Redundancy Analyses showed a taxonomic and functional response to fire as all burnt areas had more Hymenoptera families, different community composition and higher numbers of parasitoids than the unburnt area. Taxonomic differences were also found between burnt areas in terms of the response of Hymenoptera to post-fire management. In general the number of parasitoids was positively correlated to the number of potential host arthropods. Parasitoids are recognized to be sensitive to habitat changes, thus highlighting their value for monitoring the functional responses of organisms to habitat disturbance. The taxonomic and functional responses of Hymenoptera suggest that some pine-forest fires can enhance habitat heterogeneity and arthropod diversity, hence increasing interspecific interactions such as those established by parasitoids and their hosts.

The genus Synergus Hartig (Hymenoptera: Cynipidae: Synergini) in the New World: a complete taxonomic revision with a key to species.

A complete revision of the genus Synergus Hartig (Hymenoptera: Cynipidae: Synergini) in the New World (Nearctic and Neotropical regions) is conducted for the first time in order to stabilize its taxonomy. A total of 11 new species are described from Mexico: S. ashmeadi Lobato-Vila Pujade-Villar, sp. nov.; S. beutenmulleri Lobato-Vila Pujade-Villar, sp. nov.; S. compressus Lobato-Vila Pujade-Villar, sp. nov.; S. diversicolor Lobato-Vila Pujade-Villar, sp. nov.; S. ebenus Lobato-Vila Pujade-Villar, sp. nov.; S. linnei Lobato-Vila Pujade-Villar, sp. nov.; S. macrackenae Lobato-Vila Pujade-Villar, sp. nov.; S. oaxaquensis Lobato-Vila Pujade-Villar, sp. nov.; S. personatus Lobato-Vila Pujade-Villar, sp. nov.; S. ruficephalus Lobato-Vila Pujade-Villar, sp. nov.; and S. weldi Lobato-Vila Pujade-Villar, sp. nov. Synergus splendidus Fullaway, 1911 is proposed as a syn. nov. of S. dorsalis (Provacher, 1889); S. garryana Gillette, 1893 and S. oneratus coloradensis Gillette, 1896 as syn. nov. of S. oneratus (Harris, 1841); and S. magnificus Weld, 1957 as a syn. nov. of S. reniformis McCracken Egbert, 1922. Redescriptions and illustrations are provided for poorly characterized species. A key to species and a summary table including all valid Synergus from the New World, their biology and distribution, are given. Distribution, morphology, and trophic associations are discussed and compared between New World and Palaearctic species.

A new cynipid inquiline of the genus Lithosaphonecrus (Hymenoptera: Cynipidae: Synergini) from India, with an updated key to all known species.

A new species of cynipid inquiline, Lithosaphonecrus nagalandi Melika, Lobato-Vila Pujade-Villar, sp. nov. (Hymenoptera: Cynipidae: Synergini), is described from the state of Nagaland (India) reared from undescribed bud galls on an undetermined species of Lithocarpus (Fagaceae), thus being the first Lithosaphonecrus known from India. Description, diagnosis, data on phenology and host associations, and illustrations of the new species are given. An identification key to all known Lithosaphonecrus is also provided. The biology of the genus Lithosaphonecrus and the distribution range of Saphonecrus and Lithosaphonecrus in Asia and Oceania are discussed.

A Taxonomic Review of the Gall Wasp Genus Saphonecrus Dalla-Torre and Kieffer and other Oak Cynipid Inquilines (Hymenoptera: Cynipidae) from Mainland China, with Updated Keys to Eastern Palaearctic and Oriental Species.

After the examination of the oak cynipid inquilines deposited in the Parasitic Hymenoptera Collection of the Agriculture and Forestry University of Zhejiang (ZAFU, China), we provide a revision of the species of Saphonecrus, Lithosaphonecrus, Ufo (Hymenoptera: Cynipidae: Synergini) and Ceroptres (Hymenoptera: Cynipidae: Ceroptresini) found in mainland China. Two new species of Saphonecrus are described: S. albidus Lobato-Vila and Pujade-Villar, sp. nov. and S. segmentatus Lobato-Vila and Pujade-Villar, sp. nov. Four Saphonecrus species (S. gilvus Melika and Schwéger, 2015, S. globosus Schwéger and Tang, 2015, S. leleyi Melika and Schwéger, 2015, and S. nantoui Tang, Schwéger and Melika, 2015) are new records for this region. We also provide new data on the biology and distribution, redescriptions, illustrations and corrections to some of the species, as well as updated keys to Eastern Palaearctic and Oriental species of Saphonecrus and Ufo. Three species of Saphonecrus are considered to have an uncertain status: S. gemmariae (Ashmead, 1885) incertae sedis from the USA, S. excisus (Kieffer, 1904) nomen dubium from India, and S. sinicus Belizin, 1968 incertae sedis from China. The validity of Saphonecrus in the Nearctic region as well as the current status of S. serratus Weld, 1926 from the Philippines and S. favanus Weld, 1944 from the USA are discussed.

A new species of Diplolepis Geoffroy (Hymenoptera: Cynipidae: Diplolepidini) from northeastern China.

A new species, Diplolepis valtonyci Zhu, Wang Pujade-Villar sp. nova, is described from Rosa rugosa Thunb. (1784) and R. davurica Pall. (1788) from China using an integrative approach based on molecular and morphological data. Diagnosis, distribution, and biology of the new species are given and illustrated. The phylogenetic relationship between D. valtonyci sp. nova and other Diplolepis species are assessed based on COI and Cytb genes. A key to the Chinese species of Diplolepis is provided.

Three new Nearctic genera of oak cynipid gall wasps (Hymenoptera: Cynipidae: Cynipini): Burnettweldia Pujade-Villar, Melika amp; Nicholls, Nichollsiella Melika, Pujade-Villar amp; Stone, Disholandricus Melika, Pujade-Villar amp; Nicholls; and re-establishment of the genus Paracraspis Weld.

We describe three new genera of cynipid oak gall wasps from the Nearctic: Burnettweldia Pujade-Villar, Melika Nicholls, gen. nov., Nichollsiella Melika, Pujade-Villar Stone, gen. nov., and Disholandricus Melika, Pujade-Villar Nicholls, gen. nov. (Hymenoptera: Cynipidae: Cynipini). Burnettweldia includes five species, B. californicordazi Cuesta-Porta, Melika Pujade-Villar, sp. nov., B. conalis (Weld), comb. nov., B. corallina (Bassett), comb. nov., B. plumbella (Kinsey), comb. nov., B. washingtonensis (Gillette), comb. nov.. Nichollsiella includes three species, N. arizonica (Cockerell), comb. nov., N. sulcata (Ashmead), comb. nov., and N. puigi Melika, Cuesta-Porta Pujade-Villar, sp. nov.. Disholandricus includes four species, D. chrysolepidis (Ashmead), comb. nov., D. lasius (Ashmead), comb. nov., D. reniformis (McCracken Egbert), comb. nov., D. truckeensis (Ashmead), comb. nov. The genus Paracraspis Weld, comb. rev. is re-established with three species, P. guadaloupensis (Fullaway), P. insolens (Weld), and P. patelloides (Trotter). Descriptions, re-descriptions, diagnoses, keys to genera and species are given, including data on DNA sequences, biology, phenology and distribution.