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.

Sweet Tetra-Trophic Interactions: Multiple Evolution of Nectar Secretion, a Defensive Extended Phenotype in Cynipid Gall Wasps.

Many herbivores employ reward-based mutualisms with ants to gain protection from natural enemies. We examine the evolutionary dynamics of a tetra-trophic interaction in which gall wasp herbivores induce their host oaks to produce nectar-secreting galls, which attract ants that provide protection from parasitoids. We show that, consistent with other gall defensive traits, nectar secretion has evolved repeatedly across the oak gall wasp tribe and also within a single genus (Disholcaspis) that includes many nectar-inducing species. Once evolved, nectar secretion is never lost in Disholcaspis, consistent with high defensive value of this trait. We also show that evolution of nectar secretion is correlated with a transition from solitary to aggregated oviposition, resulting in clustered nectar-secreting galls, which produce a resource that ants can more easily monopolize. Such clustering is commonly seen in ant guard mutualisms. We suggest that correlated evolution between maternal oviposition and larval nectar induction traits has enhanced the effectiveness of this gall defense strategy.

Tournament ABC analysis of the western Palaearctic population history of an oak gall wasp, Synergus umbraculus.

Approximate Bayesian computation (ABC) is a powerful and widely used approach in inference of population history. However, the computational effort required to discriminate among alternative historical scenarios often limits the set that is compared to those considered more likely a priori. While often justifiable, this approach will fail to consider unexpected but well-supported population histories. We used a hierarchical tournament approach, in which subsets of scenarios are compared in a first round of ABC analyses and the winners are compared in a second analysis, to reconstruct the population history of an oak gall wasp, Synergus umbraculus (Hymenoptera, Cynipidae) across the Western Palaearctic. We used 4,233 bp of sequence data across seven loci to explore the relationships between four putative Pleistocene refuge populations in Iberia, Italy, the Balkans and Western Asia. We compared support for 148 alternative scenarios in eight pools, each pool comprising all possible rearrangements of four populations over a given topology of relationships, with or without founding of one population by admixture and with or without an unsampled "ghost" population. We found very little support for the directional "out of the east" scenario previously inferred for other gall wasp community members. Instead, the best-supported models identified Iberia as the first-regional population to diverge from the others in the late Pleistocene, followed by divergence between the Balkans and Western Asia, and founding of the Italian population through late Pleistocene admixture from Iberia and the Balkans. We compare these results with what is known for other members of the oak gall community, and consider the strengths and weaknesses of using a tournament approach to explore phylogeographic model space.

Four new species of Andricus Hartig oak gallwasp from Turkey (Hymenoptera: Cynipidae, Cynipini).

Four new species of oak gallwasps, Andricus ahmeti, A. anatolicus, A. bakrachus and A. turcicus (Hymenoptera: Cynipidae: Cynipini) are described from Turkey. All four species are known only from asexual females and induce galls on twigs and young shoots on Q. infectoria, Q. macranthera and Q. petraea. Data on the diagnosis, distribution and biology of the four new species are given. Andricus stonei and Aphelonyx kordestanica are listed for the first time for the Turkish oak gallwasp fauna.

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.

Life history, natural enemies, and management of Disholcaspis quercusvirens (Hymenoptera: Cynipidae) on live oak trees.

Live oak (Quercus virginiana Mill.) trees are hosts to a complex of gall making arthropods. However, the bullet galls produced by the asexual generation of the cynipid Disholcaspis quercuscirens (Ashmead) can esthetically and physically damage nursery and street trees, and thus reduce tree value. We sought to describe the unknown sexual generation of D. quercusvirens, describe the development of galls from both generations, record adult cynipid and parasitoid activity periods, and evaluate the efficacy of several insecticides to suppress the gall makers and prevent additional gall formation. The oviposition period for asexual females occurred from late November to January in both years of the caging study. Eggs laid into dormant buds resulted in small bud galls in which the sexual generation developed for 4-5 mo. Sexual adults emerged and laid eggs in young elongating shoots in April. Bullet galls began protruding from branches in June, and asexual wasps emerged 5-7 mo later. Cynipids that emerged from the bullet (asexual generation) and bud (sexual generation) galls were genetically identical. Both generations were heavily parasitized. Targeting asexual females with an early December treatment of bifenthrin or acephate significantly reduced the number of bud galls, but control did not extend to the next generation of bullet galls, possibly because of reinvasion from neighboring infested trees.

The description of Alloxysta chinensis, a new Charipinae species from China (Hymenoptera, Figitidae).

A new figitid species, Alloxysta chinensis Fülöp & Mikó sp nova, based on females, is described from China and South Korea. The functional morphology and the phylogenetic implication of some anatomical structures frequently used in Charipinae and the validity of the genus Carvercharips is discussed. This manuscript is the first of its kind linking descriptive terminology to Hymenoptera Anatomy Ontology classes, which provides persistent links to definitions for terms used within this manuscript.

A new genus of oak gallwasp, Cyclocynips Melika, Tang & Sinclair (Hymenoptera: Cynipidae: Cynipini), with descriptions of two new species from Taiwan.

A new genus of cynipid oak gallwasp-Cyclocynips Melika, Tang, & Sinclair (Hymenoptera: Cynipidae: Cynipini), with two new species--C. uberis and C. tumorvirgae--reared from galls on oaks of the Quercus subgenus Cyclobalanopsis is described from Taiwan. Descriptions of asexual generation adults and their diagnostic characters are presented. The likelihood of yet undiscovered sexual generations and the evolution of host-plant associations in these species are discussed.

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.

Holocynips illinoiensis, sp. nov., a new species of oak gall wasp (Hymenoptera: Cynipidae) from the USA.

A new species, Holocynips illinoiensis Melika & Nicholls, sp. nov. is described from the Nearctic (America north of Mexico). Description, diagnoses, information on biology and host association is given for the new species, as well as preliminary discussion on the coherence of the genus Holocynips.

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.

A likelihood-based comparison of population histories in a parasitoid guild.

Little is known about the stability of trophic relationships in complex natural communities over evolutionary timescales. Here, we use sequence data from 18 nuclear loci to reconstruct and compare the intraspecific histories of major Pleistocene refugial populations in the Middle East, the Balkans and Iberia in a guild of four Chalcid parasitoids (Cecidostiba fungosa, Cecidostiba semifascia, Hobbya stenonota and Mesopolobus amaenus) all attacking Cynipid oak galls. We develop a likelihood method to numerically estimate models of divergence between three populations from multilocus data. We investigate the power of this framework on simulated data, and-using triplet alignments of intronic loci-quantify the support for all possible divergence relationships between refugial populations in the four parasitoids. Although an East to West order of population divergence has highest support in all but one species, we cannot rule out alternative population tree topologies. Comparing the estimated times of population splits between species, we find that one species, M. amaenus, has a significantly older history than the rest of the guild and must have arrived in central Europe at least one glacial cycle prior to other guild members. This suggests that although all four species may share a common origin in the East, they expanded westwards into Europe at different times.

Host niches and defensive extended phenotypes structure parasitoid wasp communities.

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the "Enemy Hypothesis," which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.

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.

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 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.

A new genus of Nearctic oak gall wasp, Grahamstoneia Melika amp; Nicholls, gen. nov. (Hymenoptera: Cynipidae, Cynipini).

A new genus, Grahamstoneia Melika Nicholls, gen. nov., with one new species, G. humboldti Melika Nicholls, sp. nov., asexual generation, is described. This new taxon occurs in the south-western Nearctic, inducing galls on two species within Quercus section Protobalanus (Q. vacciniifolia Kellogg and Q. chrysolepis Liebm.), an ecology and distribution shared with the closely related genus Heteroecus Kinsey. Descriptions, diagnoses, biology, and host associations for the new genus and species are given. The new taxon is supported by morphological and molecular data.

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.