Graham N Stone

University of Edinburgh | UoE · Institute of Evolutionary Biology

In recent years, new wasp species and genera of Cynipidae have been described, and their species delimitation and evolutionary relationships have been supported using molecular markers. However, few studies have included comprehensive and extensive sampling of specimens across the complete distribution of a single genus. In this study, we analysed...

1. A key question in insect community ecology is whether parasitoid assemblages are structured by the food plants of their herbivore hosts. 2. Tritrophic communities centred on oak-feeding cynipid gallwasps are one of the best-studied tritrophic insect communities. Previous work suggests that host plant identity is a much stronger predictor of oak...

Revealing processes that structure species interactions is central to understanding community assembly and dynamics. Species interact via their phenotypes, but identifying and quantifying the traits that structure species-specific interactions (links) can be challenging. Where these traits show phylogenetic signal, however, link properties may be p...

Most animal pollination results from plant–insect interactions, but how we perceive these interactions may differ with the sampling method adopted. The two most common methods are observations of visits by pollinators to plants and observations of pollen loads carried by insects. Each method could favour the detection of different species and inter...

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 (...

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...

Gall 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 transcript...

Context Agri-environment schemes support land management interventions that benefit biodiversity, environmental objectives, and other public goods. Process-based model simulations suggest the English scheme, as implemented in 2016, increased wild bee pollination services to pollinator-dependent crops and non-crop areas in a geographically heterogen...

Insects provide key pollination services in most terrestrial biomes, but this service depends on a multistep interaction between insect and plant. An insect needs to visit a flower, receive pollen from the anthers, move to another conspecific flower, and finally deposit the pollen on a receptive stigma. Each of these steps may be affected by climat...

During the main COVID-19 global pandemic lockdown period of 2020 an impromptu set of pollination ecologists came together via social media and personal contacts to carry out standardised surveys of the flower visits and plants in gardens. The surveys involved 67 rural, suburban and urban gardens, of various sizes, ranging from 61.18° North in Norwa...

Ant guards can increase plant fitness by deterring herbivores, but they may also reduce it by interfering with pollination. While ant impacts on herbivory have been well‐studied, much less is known about their impacts on pollinators and associated consequences for plant pollination, particularly pollen transfer dynamics and outcrossing/selfing rate...

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. Thi...

Cryptic species diversity is a major challenge for 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...

The phylogeny of gall wasps (Cynipidae) and their parasitic relatives has attracted considerable attention in recent years. The family is now widely recognized to fall into thirteen natural lineages, designated tribes, but the relationships among them have remained elusive. This has stymied any progress in understanding how cynipid gall inducers ev...

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, diagnose...

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 generati...

A new species of oak gall wasp, Andricus pseudocecconii Melika, Tavakoli & Stone, sp. nov. (Hymenoptera: Cynipidae, Cynipini) is described. Descriptions, diagnoses, biology, and host associations for the new species are given. The new taxon is supported by morphological and molecular data.

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 (Beutenmüller), comb. nov., D. garciamartinonae Pujade-Villar, sp. nov., D. grego...

In forests, insect herbivores and their host plants are major components of the community. The study of their interactions is essential for understanding the mechanisms promoting and maintaining species diversity and niche differentiation in both trophic levels (Becerra 2015). Theory has long predicted that the evolution of plant anti-herbivore def...

Plant galls are novel and sometimes dramatic plant organs whose development is initiated and controlled by parasitic microbes, nematodes, insects and mites. For arthropods, galls provide relative safety from enemies and abiotic stresses while providing nutrition (Stone and Schonrogge 2003). Galls are formed entirely by the plant, whose transcriptio...

Agri-environment schemes are programmes where landholders enter into voluntary agreements (typically with governments) to manage agricultural land for environmental protection and nature conservation objectives. Previous work at local scale has shown that these features can provide additional floral and nesting resources to support wild pollinators...

Cryptic species diversity is a major challenge for 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...

Twenty nine new species of cynipid oak gall wasps from the Nearctic region (America north of Mexico) are described: Andricus archboldi Melika & Abrahamson, sp. nov., A. catalinensis Melika, Nicholls & Stone, sp. nov., A. chapmanii Melika & Abrahamson, sp. nov., A. chiricahuensis Melika, Nicholls & Stone, sp. nov., A. coconinoensis Melika, Nicholls...

A new genus, Prokius Nieves Aldrey, Medianero & Nicholls, gen. nov., and two new species of oak gall wasps (Hymenoptera: Cynipidae: Cynipini), Prokius cambrai Medianero & Nieves-Aldrey sp. nov. and Prokius lisethiae Medianero & Nieves-Aldrey sp. nov., are described from adults reared from galls on Quercus bumelioides Liebm (Fagaceae, sect. Quercus,...

Climate change is advancing the onset of phenological events, with the rate of advance varying among species and trophic levels. In addition, local populations of the same species may show genetic differences in their response to seasonal cues. If populations of interacting species differ in their response, then climate change may result in geograp...

Floral resources are a key driver of pollinator abundance and diversity, yet their quantification in the field and laboratory is laborious and requires specialist skills. Using a dataset of 25,000 labelled tags of fieldwork‐realistic quality, a convolutional neural network (Faster R‐CNN) was trained to detect the nectar‐producing floral units of 25...

This is a two page infographic summary of the main paper aimed at policymakers and staff who simply don't have the time to readv the full paper. Please feel free to pass it around.

Pollinators experience large spatiotemporal fluctuations in resource availability when mass‐flowering crops are rotated with resource‐poor cereal crops. Yet, few studies have considered the effect this has on pollinator population stability, nor how this might be mitigated to maintain consistent crop pollination services. We assess the potential of...

Evolutionary processes in ant-plant mutualisms are mediated by intrinsic features of the association and by change through time in abiotic components of the system (e.g. geography and climate). Incorporating both biotic and abiotic components and the phylogenies of the taxa involved is central to understanding their respective roles in mutualism ev...

Signatures of past changes in population size have been detected in genome-wide variation in many species. However, the causes of such demographic changes and the extent to which they are shared across co-distributed species remain poorly understood. During Pleistocene glacial maxima, many temperate European species were confined to southern refugi...

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 Cuest...

Signatures of past changes in population size have been detected in genome-wide variation in many species. However, the causes of such demographic changes and the extent to which they are shared across co-distributed species remain poorly understood. During Pleistocene glacial maxima, many temperate European species were confined to southern refugi...

We provide a checklist of the gall wasps (Hymenoptera: Cynipidae: Cynipinae) of Iran, and place these records in a biogeographical perspective on three spatial scales, comprising (i) the Western Palaearctic, (ii) Western Asia (Turkey, the southern Caucasus and the Middle East) and (iii) regions within Iran. We present distribution and biological da...

The monophyly and taxonomic validity of some currently accepted genera of gall wasps in the Cynipini (Hymenoptera: Cynipidae) are being challenged by recent systematic studies. Here we used morphological and molecular data to re-describe and revise the taxonomic limits of the monotypic genus Kokkocynips Pujade-Villar & Melika, previously recorded o...

Floral resources (nectar and pollen) provide food for insect pollinators but have declined in the countryside due to land use change. Given widespread pollinator loss, it is important that we quantify their food supply to help develop conservation actions. While nectar resources have been measured in rural landscapes, equivalent data are lacking fo...

This is a two page infographic version of the paper itself, designed for non-acedemic readers. Please feel free to distribute widely

A new species of inquiline, Lithosaphonecrus edurus Fang, Melika, and Tang, new species (Hymenoptera: Cynipidae: Synergini) is described from Emeishan, Sichuan Province, China. Lithosaphonecrus edurus is associated with an as yet undetermined cynipid gall on Lithocarpus cleistocarpus var. cleistocarpus and var. omeiensis, L. hancei and L. megalophy...

The known species richness of oak gallwasps in Asia has increased tremendously in the past decade. However, the vast majority of taxa have been described from the east coast of Asia, and knowledge of oak gallwasps from Central Asia is still scant. Here we use molecular and morphological characters to describe a new genus of cynipid oak gallwasp, He...

1. Pollination is a key ecosystem service for global agriculture but evidence of polli-nator population declines is growing. Reliable spatial modelling of pollinator abundance is essential if we are to identify areas at risk of pollination service deficit and effectively target resources to support pollinator populations. Many models exist which pr...

Gall wasps (Hymenoptera: Cynipidae) induce complex galls on oaks, roses and other plants, but the mechanism of gall induction is still unknown. Here we take a comparative genomic approach to revealing the genetic basis of gall induction. We focus on Synergus itoensis, a species that induces galls inside oak acorns. Previous studies suggested that t...

Population divergence and gene flow are key processes in evolution and ecology. Model‐based analysis of genome‐wide datasets allows discrimination between alternative scenarios for these processes even in non‐model taxa. We used two complementary approaches (one based on the blockwise site frequency spectrum (bSFS), the second on the Pairwise Seque...

[This corrects the article DOI: 10.1371/journal.pgen.1007533.].

Little is known about the dietary richness and variation of generalist insectivorous species, including birds, due primarily to difficulties in prey identification. Using faecal metabarcoding we provide the most comprehensive analysis of a passerine's diet to date, identifying the relative magnitudes of biogeographic, habitat and temporal trends in...

Population divergence and gene flow are key processes in evolution and ecology. Model-based analysis of genome-wide datasets allows discrimination between alternative scenarios for these processes even in non-model taxa. We used two complementary approaches (one based on the blockwise site frequency spectrum (bSFS), the second on the Pairwise Seque...

Ant guards can increase plant fitness by deterring herbivores but may also reduce it by interfering with pollination, hence ant-plant interactions are ideal systems in which to study costs and benefits of mutualisms. While ant impacts on herbivory are well-studied, much less is known about impacts on pollinators and associated consequences for plan...

Signatures of changes in population size have been detected in genome-wide variation in many species. However, the causes of such changes and the extent to which they are shared across co-distributed species remain poorly understood. During Pleistocene glacial maxima, many temperate European species were confined to southern refugia. While vicarian...

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...

Although vertebrates have been reported to gain higher reproductive outputs by choosing mates, few studies have been conducted on threatened species. However, species recovery should benefit if natural mate choice could improve reproductive output (i.e. pair performance related to offspring number, such as increased clutch size, numbers of fertiliz...

To gain insight into wasp factors that might be involved in the initial induction of galls on woody plants, we performed high throughput (454) transcriptome analysis of ovaries and venom glands of two cynipid gall wasps, Biorhiza pallida and Diplolepis rosae, inducing galls on oak and rose, respectively. De novo assembled and annotated contigs were...

This study uses an integrated approach to address the taxonomic status of six different and problematic oak galls and their inducing wasps sampled from two sites in the Central Zagros Mountains (Lorestan province) in western Iran. Our aim was to establish whether morphologically similar but different galls are induced by the same or distinct gall-i...

Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyr...

Ant guards protect plants from herbivores, but can also hinder pollination by damaging reproductive structures and/or repelling pollinators. Natural selection should favour the evolution of plant traits that deter ants from visiting flowers during anthesis, without waiving their defensive services. The Distraction Hypothesis posits that rewarding a...

Urban areas are often perceived to have lower biodiversity than the wider countryside, but a few small-scale studies suggest that some urban land uses can support substantial pollinator populations. We present a large-scale, well-replicated study of floral resources and pollinators in 360 sites incorporating all major land uses in four British citi...

Four species of Dryocosmus cynipid gallwasps are now known to induce galls on Chrysolepis in California and Oregon. Two new species, Dryocosmus demartinii Melika, Nicholls & Stone and Dryocosmus juliae Melika, Nicholls & Stone are described. Males of the sexual generation of D. rileypokei plus adults of the asexual generation of this species are bo...

In the last paragraph of the Origin of Species, Darwin (1859) marvels at the diversity of life forms, the complexity of links between them, and the forces creating this “tangled bank”. In this text, we may see the origins of community ecology – today defined as ‘the study of the interactions that determine the distribution and abundance of organism...

We describe a new genus of cynipid oak gallwasp, Protobalandricus Melika, Nicholls & Stone (Hymenoptera: Cynipidae: Cynipini). Protobalandricus gen. nov. includes one previously described species, Disholcaspis spectabilis (Kinsey), which induces stem swelling-like galls on golden cup oaks, Quercus section Protobalanus. Descriptions of the genus and...

Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of pla...

MrBayes majority-rule consensus tree for the nuclear locus wingless, sequenced for exemplars of each of the selected 41 jMOTU 1.5% COI MOTUs. Numbers above nodes indicate posterior probabilities. Taxon labels are colored to indicate membership of different MOTUs.

List of compounds putatively identified through matches to reference MSMS spectra on the Global Natural Products Social Molecular Networking database (https://gnps.ucsd.edu/ProteoSAFe/static/gnps-splash.jsp). The cosine score is a measure of the similarity of MS/MS-derived fragments between two compounds.

Detailed chemical methods for construction of a chemical similarity matrix.

MrBayes majority-rule consensus tree for the mitochondrial COI DNA barcode fragment. Numbers above nodes indicate posterior probabilities. Taxon label colors indicate membership of 1.5% sequence divergence jMOTU taxa, indicated by the labels at right.

MrBayes majority-rule consensus tree for the nuclear locus ITS2, sequenced for exemplars of each of the selected 41 jMOTU 1.5% COI MOTUs. Numbers above nodes indicate posterior probabilities. Taxon labels are colored to indicate membership of different MOTUs.

Phylogenetic relationships for the gene CO1 among the Inga-feeding sawfly MOTUs and a panel of voucher sequences for sawflies in the families Argidae, Pergidae (sister group to Argidae; Malm and Nyman, 2015) and Tenthredinidae. The tree shown is a majority-rule consensus tree constructed in MrBayes, using substitutions modeled as GTR+I+G for each o...

Metadata for additional reference sawfly sequences, with species name, country of origin, Genbank accession numbers for COI and PGD gene fragments, and source reference.

Information on the ten sequence loci used for construction of the Inga species tree. Locus number, reference transcript, functional annotation and the substitution model used in phylogenetic analyses all refer to Nicholls et al. (2015).

Results of MOTU identification analyses of Inga- and Zygia-feeding sawflies, using a 645 bp fragment of the mitochondrial COI DNA barcoding region for (a) jMOTU and (b) ABGD.

Parafit analysis output for sawfly and Inga phylogenies, for sawfly MOTUs in the family Argidae. (B) Parafit analysis of concordance between sawfly phylogeny and Inga chemogram. In (A) and (B) herbivore-Inga associations that are identified as individually significant are highlighted in yellow.

Sawfly MOTU accumulation curves when sampling over Inga host plant taxa, and when sampling over individuals. For each curve, the mean estimate is shown as a dark blue line and the standard deviation as a pale blue shaded region either side. The total numbers of Inga taxa and sawfly specimens in these analyses were 34 and 1286, respectively.