J. L. Nieves-Aldrey

Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes

Little is known about the evolutionary history of most complex multi‐trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host‐tracking) or later divergence in higher trophic levels (Delayed Host‐tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species‐level divergence at both 8–9 and 4–5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host‐tracking Hypothesis for community evolution.

Longitudinal range expansion and cryptic eastern species in the western Palaearctic oak gallwasp, Andricus coriarius

The oak gallwasp Andricus coriarius is distributed across the Western Palaearctic from Morocco to Iran. It belongs to a clade of host‐alternating Andricus species that requires host oaks in two sections of Quercus subgenus Quercus to complete its lifecycle, a requirement that has restricted the historic distribution and dispersal of members of this clade. Here we present nuclear and mitochondrial sequence evidence from the entire geographic range of A. coriarius to investigate the genetic legacy of longitudinal range expansion. We show A. coriarius as currently understood to be para‐ or polyphyletic, with three evolutionarily independent (but partially sympatric) lineages that diverged c. 10 million years ago (mya). The similarities in gall structure that have justified recognition of single species to date thus represent either strong conservation of an ancestral state or striking convergence. All three lineages originated in areas to the east of Europe, underlining the significance of Turkey, Iran and the Levant as ‘cradles’ of gallwasp evolution. One of the three lineages gave rise to all European populations, and range expansion from a putative Eastern origin to the present distribution is predicted to have occurred around 1.6 mya.

The incidence and diversity of Wolbachia in gallwasps (Hymenoptera; Cynipidae) on oak.

Wolbachia bacteria infect ≈ 20% of all insect species, and cause a range of alterations to host reproduction, including imposition of thelytoky. The incidence and phenotypic impact of Wolbachia remains to be established in many insect taxa, and considerable research effort is currently focused on its association with particular reproductive modes and the relative importance of the various pathways via which infection occurs. Gallwasps represent an attractive system for addressing these issues for two reasons. First, they show a diversity of reproductive modes (including arrhenotoky, thelytoky and cyclical parthenogenesis) in which the impact of Wolbachia infection can be examined. Second, they occupy two intimately linked trophic niches (gall‐inducers and inquilines) between which there is potential for the horizontal exchange of Wolbachia infection. In the arrhenotokous gallwasp lineages screened to date (the herb‐galling ‘Aylacini’ and the rose‐galling Diplolepidini), Wolbachia infection always induces thelytoky. The impact of Wolbachia in other arrhenotokous clades, and in the cyclically parthenogenetic clades remains unknown. Here we use polymerase chain reaction (PCR) screening and sequence data for two Wolbachia genes (wsp and ftsZ) to examine the prevalence and incidence of Wolbachia infection in 64 species (a total of 609 individuals) in two further tribes: the arrhenotokous inquilines (tribe Synergini), and the cyclically parthenogenetic oak gallwasps (tribe Cynipini). We ask: (i) whether Wolbachia infection has any apparent impact on host reproduction in the two tribes and (ii) whether there is any correlation between Wolbachia infection and the apparent lack of an arrhenotokous generation in many oak gallwasp life cycles. We show: (i) that Wolbachia infection is rare in the Cynipini. Infected species show no deviation from cyclical parthenogenesis, and infection is no more common in species known only from a thelytokous generation; (ii) that there is a higher incidence of infection within the arrhenotokous inquilines, and generally in gallwasp tribes without cyclical parthenogensis; (iii) all Wolbachia‐positive inquiline species are known to possess males, implying either that Wolbachia infection does not result in loss of sex in this tribe or, more probably, that (as for some rose gallwasps) Wolbachia infection leads to loss of sex in specific populations; and (iv) although we find some inquilines and gall inducers to be infected with Wolbachia having the same wsp sequence, these hosts are not members of the same gall communities, arguing against frequent horizontal transmission between these two trophic groups. We suggest that exchange may be mediated by the generalist parasitoids common in oak galls.

Phylogeny, Evolution and Classification of Gall Wasps: The Plot Thickens

Gall wasps (Cynipidae) represent the most spectacular radiation of gall-inducing insects. In addition to true gall formers, gall wasps also include phytophagous inquilines, which live inside the galls induced by gall wasps or other insects. Here we present the first comprehensive molecular and total-evidence analyses of higher-level gall wasp relationships. We studied more than 100 taxa representing a rich selection of outgroups and the majority of described cynipid genera outside the diverse oak gall wasps (Cynipini), which were more sparsely sampled. About 5 kb of nucleotide data from one mitochondrial (COI) and four nuclear (28S, LWRh, EF1alpha F1, and EF1alpha F2) markers were analyzed separately and in combination with morphological and life-history data. According to previous morphology-based studies, gall wasps evolved in the Northern Hemisphere and were initially herb gallers. Inquilines originated once from gall inducers that lost the ability to initiate galls. Our results, albeit not conclusive, suggest a different scenario. The first gall wasps were more likely associated with woody host plants, and there must have been multiple origins of gall inducers, inquilines or both. One possibility is that gall inducers arose independently from inquilines in several lineages. Except for these surprising results, our analyses are largely consistent with previous studies. They confirm that gall wasps are conservative in their host-plant preferences, and that herb-galling lineages have radiated repeatedly onto the same set of unrelated host plants. We propose a revised classification of the family into twelve tribes, which are strongly supported as monophyletic across independent datasets. Four are new: Aulacideini, Phanacidini, Diastrophini and Ceroptresini. We present a key to the tribes and discuss their morphological and biological diversity. Until the relationships among the tribes are resolved, the origin and early evolution of gall wasps will remain elusive.

Gall wasp community response to fragmentation of oak tree species: importance of fragment size and isolated trees

We explore the impact of habitat fragmentation on interactions between keystone resources of forest trees—oaks, genus Quercus (Fagaceae)—and an associated radiation of specialist cynipid gall wasps. Habitat fragmentation is predicted to have bottom-up impacts on cynipid communities through impacts on host plant quality (plant vigor hypothesis). We explored the bottom-up impacts on cynipid communities of habitat fragment size, fragment edge effects and presence of isolated oaks. We quantified temporal and spatial variation of leaves produced in the canopy to quantify plant vigor, and surveyed cynipid gall species abundance and richness over three years using 15 permanent forest patches and 25 isolated oaks in a fragmented oak woodland landscape in central Mexico. Cynipid gall abundance and species richness were higher in isolated oaks and small woodland fragments than in larger ones. Cynipid abundance and species richness were also higher along fragment edges in comparison with fragment interiors. This contrasts with patterns observed in other taxa. In addition, host plant quality was higher in isolated trees, in smaller fragments and along fragment edges. We therefore hypothesize that observed patterns in cynipid abundance and species richness are driven by changes in host plant quality due to forest fragmentation. Our data represent a baseline for longer-term monitoring of fragmentation effects at a landscape scale. Further work is required to explore alternative potential explanations for observed patterns, including the estimation of potential top-down impacts of fragmentation mediated by natural enemies.

First evidence of cynipids from the Oceanian Region: the description of Lithonecrus papuanus a new genus and species of cynipid inquiline from Papua New Guinea (Hymenoptera: Cynipidae, Synergini).

Lithonecrus papuanus Nieves-Aldrey & Butterill, a new genus and species of inquiline oak gall wasps (Hymenoptera: Cynipidae: Synergini), is described from material reared from galls on Lithocarpus celebicus (Miq.) Rehd., collected in Papua New Guinea. The new genus and species is the first record of a cynipid from Papua New Guinea and the wholexa0 Oceanian biogeographic region,xa0 and represents the easternmost oriental record of a cynipid wasp (Hymenoptera: Cynipidae). The new genus is similar to Saphonecrus Dalla Torre & Kieffer, and to the recently described Lithosaphonecrus Tang, Melika & Bozsó, but differs from these genera in several important diagnostic characters. Taxonomic affinities and differences with related genera and species and biogeographical implications are discussed.xa0

Variation in the species richness of parasitoid wasps (Ichneumonidae: Pimplinae and Rhyssinae) across sites on different continents

The old idea that parasitoid wasps (Ichneumonidae) show an inverse latitudinal diversity gradient has recently been challenged, but how ichneumonid species richness varies across the globe is still not well understood. We carried out field inventories in 21 sites on three continents to clarify this question, focusing on the subfamilies Pimplinae and Rhyssinae. Our total sampling effort was 628 Malaise trap months and the total catch exceeded 65 000 individuals. Our main focus was in two intensively inventoried areas in Amazonia, together yielding 257 Malaise trap months and 26 390 ichneumonid individuals. To expand the scope and assess global species diversity patterns of the Pimplinae and Rhyssinae, we compiled published species lists from a total of 97 study localities around the world. The highest observed species richness in any locality, 105 species, was found in one of our field sites in Peruvian Amazonia. None of the other localities reported more than 70 species, even the ones with a sampling effort comparable to ours. Despite the local thoroughness of our field inventories in Amazonia, data analyses indicated that a substantial proportion of the parasitoid wasp species occurring in each site remained unobserved. The highest local species richness values were reported from the tropics. Nevertheless parasitoid wasps are still too sparsely sampled to draw solid conclusions about whether or not their species richness follows a particular latitudinal trend, and if so, where their richness peaks.