José Luis Nieves-Aldrey

Bayesian phylogenetic analysis of combined data.

The recent development of Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) techniques has facilitated the exploration of parameter-rich evolutionary models. At the same time, stochastic models have become more realistic (and complex) and have been extended to new types of data, such as morphology. Based on this foundation, we developed a Bayesian MCMC approach to the analysis of combined data sets and explored its utility in inferring relationships among gall wasps based on data from morphology and four genes (nuclear and mitochondrial, ribosomal and protein coding). Examined models range in complexity from those recognizing only a morphological and a molecular partition to those having complex substitution models with independent parameters for each gene. Bayesian MCMC analysis deals efficiently with complex models: convergence occurs faster and more predictably for complex models, mixing is adequate for all parameters even under very complex models, and the parameter update cycle is virtually unaffected by model partitioning across sites. Morphology contributed only 5% of the characters in the data set but nevertheless influenced the combined-data tree, supporting the utility of morphological data in multigene analyses. We used Bayesian criteria (Bayes factors) to show that process heterogeneity across data partitions is a significant model component, although not as important as among-site rate variation. More complex evolutionary models are associated with more topological uncertainty and less conflict between morphology and molecules. Bayes factors sometimes favor simpler models over considerably more parameter-rich models, but the best model overall is also the most complex and Bayes factors do not support exclusion of apparently weak parameters from this model. Thus, Bayes factors appear to be useful for selecting among complex models, but it is still unclear whether their use strikes a reasonable balance between model complexity and error in parameter estimates.

Differential success in northwards range expansion between ecotypes of the marble gallwasp Andricus kollari: A tale of two lifecycles

The Marble gallwasp Andricus kollari has a native range divided into two geographically separated lifecycles. In Eastern Europe and Turkey, the lifecycle involves a sexual generation on Turkey oak, Quercus cerris, while in Iberia and North Africa the sexual generation host is cork oak, Q. suber. Over the last 500 years, A. kollari has expanded its range into northern Europe, following human planting of Q. cerris from Italy and the Balkans. We ask: (i) what is the genetic relationship between eastern and western distributions of Andricus kollari? Can we determine which lifecycle is ancestral, and how long ago they diverged? (ii) To what extent have eastern and western native ranges contributed to northwards range expansion? (iii) Is there any evidence for hybridization between the two life cycle types? We present analyses of allozyme data for 13 polymorphic loci and of sequence variation for a 433 bp fragment of the mitochondrial cytochrome b gene. These show: (i) that four haplotype lineages (one in Spain, two in Hungary/Italy and one in Turkey) diverged more or less simultaneously between 1 and 2 million years ago, suggesting the existence of at least four refuges through recent ice age cycles. Our data cannot resolve which lifecycle type is ancestral. (ii) Populations north of putative refuges are divided into two sets. Populations in south‐west France are allied to Spain, while all remaining populations in northern Europe have been colonized from Italy and the Balkans. (iii) The transition from one race to another in south‐west France is marked by abrupt transitions in the frequency of refuge‐specific private alleles and corresponds closely to the northern limit of the distribution of cork oak. Although hybrids were detected in north‐west France, none were detected where the two lifecycles meet in south‐western France. The biology of oak gallwasps predicts that any hybrid zone will be narrow, and limited to regions where Q. cerris and Q. suber meet. Our data suggest that eastern and western A. kollari are effectively separate species.

Reconstructing Community Assembly in Time and Space Reveals Enemy Escape in a Western Palearctic Insect Community

How geographically widespread biological communities assemble remains a major question in ecology. Do parallel population histories allow sustained interactions (such as host-parasite or plant-pollinator) among species, or do discordant histories necessarily interrupt them? Though few empirical data exist, these issues are central to our understanding of multispecies evolutionary dynamics. Here we use hierarchical approximate Bayesian analysis of DNA sequence data for 12 herbivores and 19 parasitoids to reconstruct the assembly of an insect community spanning the Western Palearctic and assess the support for alternative host tracking and ecological sorting hypotheses. We show that assembly occurred primarily by delayed host tracking from a shared eastern origin. Herbivores escaped their enemies for millennia before parasitoid pursuit restored initial associations, with generalist parasitoids no better able to track their hosts than specialists. In contrast, ecological sorting played only a minor role. Substantial turnover in host-parasitoid associations means that coevolution must have been diffuse, probably contributing to the parasitoid generalism seen in this and similar systems. Reintegration of parasitoids after host escape shows these communities to have been unsaturated throughout their history, arguing against major roles for parasitoid niche evolution or competition during community assembly.

Lifecycle closure, lineage sorting, and hybridization revealed in a phylogenetic analysis of European oak gallwasps (Hymenoptera: Cynipidae: Cynipini) using mitochondrial sequence data

Oak gallwasps are cyclically parthenogenetic insects that induce a wide diversity of highly complex species- and generation-specific galls on oaks and other Fagaceae. Phylogenetic relationships within oak gallwasps remain to be established, while sexual and parthenogenetic generations of many species remain unpaired. Previous work on oak gallwasps has revealed substantial intra-specific variation, particularly between regions known to represent discrete Pleistocene glacial refuges. Here we use statistical phylogenetic inference methods on sequence data for a fragment of the mitochondrial cytochrome b gene to reconstruct the relationships among 62 oak gallwasp species. For 16 of these we also include 23 additional cytochrome b haplotype sequences from different Pleistocene refuge areas to test the effect of intra-specific variation on inter-specific phylogeny reconstruction. The reconstructed phylogenies show good intra-generic resolution and identify several conserved clades, but fail to reconstruct either very recent or very ancient divergences. Nine of the 16 species represented by multiple haplotypes are not monophyletic. The apparent discordance between the recovered gene tree and the current taxonomic classification can be explained through: (a) collapsing of some species currently known only from either a sexual or a parthenogenetic generation into a single cyclically parthenogenetic entity; (b) sorting of ancestral polymorphism in diverging lineages, and (c) horizontal transfer of haplotypes, perhaps due to hybridization within glacial refuges. Our conclusions emphasise the need for careful intra-specific sampling when reconstructing phylogenies for radiations of closely related species and imply that for certain taxonomic groups full phylogenetic resolution (using molecular markers) may not be attainable.

Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic.

We examine phylogenetic relationships within the Synergus complex of herbivorous inquiline gallwasps (Hymenoptera; Cynipidae; Synergini) associated with cynipid host galls on oak, a biologically diverse group whose genus-level morphological taxonomy has long been considered stable but whose species level taxonomy is problematic. We incorporate data for over 70% of recognised Western Palaearctic species in five morphology-based genera (Ceroptres, Saphonecrus, Synergus, Synophrus, Ufo), comprising sequence for two mitochondrial loci (coxI, cytb) and one nuclear locus (28S D2). In particular, we assess the evidence for monophyly of two long-established, morphology-defined sections within the genus Synergus that differ in a range of biological traits. To aid analyses of ecological interactions within oak cynipid communities, we also consider the utility of cytochrome oxidase I (coxI) DNA barcodes in the oak inquilines. In this assessment, we do not assume that species are delineated at a single threshold value of sequence divergence for a single gene, but examine concordance in the composition of molecular operational Taxonomic units (MOTUs) across a range of sequence divergences in each gene and across genes. We also assess the impact of sampling effort on MOTU stability. Phylogenetic reconstructions for all three loci support monophyly for Synergus and Synophrus, but reject monophyly for Saphonecrus and for the two sections within Synergus. The suites of traits associated with the two sections of the genus Synergus are thus homoplasious. All three loci also reject monophyly for three Synergus species (S. hayneanus, S. pallipes, S. umbraculus). Sequences for each locus identify robust MOTUs that are largely concordant across loci for a range of cut-off values. Though many MOTUs correspond to recognised Linnean species, there is significant, multigene disagreement between groupings supported by morphology and sequence data, with both allocation of different morphospecies to the same MOTU and allocation of the same morphospecies to multiple MOTUs, regardless of cut-off value. Our results imply that while DNA barcoding has considerable utility within this group, morphology-based identification needs major revision at both genus and species levels. Further, lifehistory traits currently attributed to single morphospecies probably confound attributes of multiple lineages. Revealing patterns of character state evolution in Synergus requires collection of new host association and life history data explicitly linked to DNA barcode data for the specimens concerned.

Comparative morphology of terminal-instar larvae of Cynipoidea: phylogenetic implications

We describe the external morphology of the terminal‐instar larvae of 30 species of Cynipoidea (Hymenoptera), with special reference to the head capsule and mouthparts. Twenty‐five of the species belong to the Cynipidae and are gall inducers or phytophagous inquilines (guests) in galls, while five represent different insect‐parasitic lineages of the Cynipoidea. Although we find only limited variation in body shape, the head sclerites and mandibles offer many characters of potential phylogenetic value. For instance, the mandibles of the parasitoids have one large pointed tooth, with several smaller dents along the inner margin in core figitids, whereas the phytophagous gall inducers and inquilines have mandibles with two or three blunt teeth of subequal size. The mandibles of inquiline larvae are unique in being covered by vertical striations and in having a dominating, broad second tooth. We summarize the qualitative variation among the studied terminal‐instar larvae in terms of 33 morphological characters and one life‐history trait and examine the phylogenetic implications of these data by running parsimony analyses under uniform character weights and under implied weights (Goloboff weights). The analysis under uniform weights is poorly resolved but the relationships suggested by the implied‐weights analysis are largely congruent with previous analyses of adult morphology and molecular data. The larval data support inclusion of the genus Liposthenes in the Neaylax–Isocolus clade, in agreement with the molecular data but in weak conflict with adult morphology. However, the larval data agree with adult morphology and conflict with the molecular data in supporting monophyly of the inquilines.

A new subfamily of Figitidae (Hymenoptera, Cynipoidea)

Larvae of the parasitic wasp family Figitidae develop as internal parasitoids of other endopterygote insect larvae. The hosts are typically dipteran larvae living in other microhabitats but the earliest figitids probably attacked gallinhabiting hymenopteran larvae. Here, we formally describe a new genus (Parnips) and subfamily (Parnipinae) for a species that is likely to be a surviving representative of these early gall-associated figitids. The species, P. nigripes, has been reared repeatedly from galls inside the seed capsules of annual poppies (Papaver dubium and P. rhoeas) in the Mediterranean region together with the gall inducer Barbotinia oraniensis belonging to the Cynipidae, the sister group of Figitidae. Parnips nigripes is strikingly cynipid-like and was first assumed to be a cynipid gall inducer of the genus Aulacidea. Phylogenetic analyses have since indicated that the similarity with the Cynipidae is symplesiomorphic and that P. nigripes belongs to the Figitidae, where it forms the sister group of all other extant figitids. Recently, it has also been shown that P. nigripes is a parasitoid of the gall-inducing Barbotinia oraniensis, consistent with its proposed phylogenetic position. Parnips nigripes shares several unusual morphological traits with its host. We speculate that many of these similarities are homologous even though the lineages separated at least 83 million years ago.  2001 The Linnean Society of London

Breaking up the wall: metal-enrichment in Ovipositors, but not in mandibles, co-varies with substrate hardness in gall-wasps and their associates.

The cuticle of certain insect body parts can be hardened by the addition of metals, and because niche separation may require morphological adaptations, inclusion of such metals may be linked to life history traits. Here, we analysed the distribution and enrichment of metals in the mandibles and ovipositors of a large family of gall-inducing wasps (Cynipidae, or Gall-Wasps) (plus one gall-inducing Chalcidoidea), and their associated wasps (gall-parasitoids and gall-inquilines) (Cynipidae, Chalcidoidea and Ichneumonoidea). Both plant types/organs where galls are induced, as well as galls themselves, vary considerably in hardness, thus making this group of wasps an ideal model to test if substrate hardness can predict metal enrichment. Non-galler, parasitic Cynipoidea attacking unconcealed hosts were used as ecological “outgroup”. With varying occurrence and concentration, Zn, Mn and Cu were detected in mandibles and ovipositors of the studied species. Zn tends be exclusively concentrated at the distal parts of the organs, while Mn and Cu showed a linear increase from the proximal to the distal parts of the organs. In general, we found that most of species having metal-enriched ovipositors (independently of metal type and concentration) were gall-invaders. Among gall-inducers, metals in the ovipositors were more likely to be found in species inducing galls in woody plants. Overall, a clear positive effect of substrate hardness on metal concentration was detected for all the three metals. Phylogenetic relationships among species, as suggested by the most recent estimates, seemed to have a weak role in explaining metal variation. On the other hand, no relationships were found between substrate hardness or gall-association type and concentration of metals in mandibles. We suggest that ecological pressures related to oviposition were sufficiently strong to drive changes in ovipositor elemental structure in these gall-associated Hymenoptera.

The importance of beta diversity in local gall-inducing arthropod distribution

Many studies over the past twenty years have documented the richness of arthropod galling species around the world, and some have proposed hypotheses to explain local and global patterns of galling species richness. However, few studies have been directed toward understanding how the gall-inducing species are locally distributed. The aim of this study was to determine the distribution of gall-inducing arthropods species at Coiba National Park, a tropical habitat on the Pacific coast of Panama. Our results suggest that more gall-inducing species had an aggregated distribution, and gall-inducing arthropod diversity shows a strong beta diversity component. Geographic distance was not correlated with similarity in gall-inducing species composition between the studied sites. This fact has important implications when trying to estimate gall-inducing arthropod richness and general patterns, and could cause contradictory results for hypotheses that attempt to explain the local and global patterns of galling species richness.

Comparative morphology and biology of terminal-instar larvae of some Eurytoma (Hymenoptera, Eurytomidae) species parasitoids of gall wasps (Hymenoptera, Cynipidae) in western Europe

Gómez J. F., Nieves-Aldrey J. L., Hernández Nieves M. & Stone G. N. 2011. — Comparative morphology and biology of terminal-instar larvae of some Eurytoma (Hymenoptera, Eurytomidae) species parasitoids of gall wasps (Hymenoptera, Cynipidae) in western Europe. Zoosystema 33 (3): 287-323. ABSTRACT We present a taxonomic and biological study of the genus Eurytoma Illiger, 1807 (Hymenoptera, Eurytomidae), based on the morphology and biology of the terminal-instar larvae of 13 species living as parasitoids in the galls of European species of cynipid gall wasps. We provide the first detailed descriptions of the terminal-instar larvae of the studied species, illustrating diagnostic characters for the family and the studied genera with SEM pictures. We also provide a species key for the identification of Eurytoma larvae associated with cynipid galls, based on particular characters associated with the head, mouthparts and mandibles. Although we find only limited informative variation in body shape, the head and mandibles provide many characters of potential taxonomic and phylogenetic value. We summarise the larval biology of the 13 Eurytoma species inhabiting cynipid galls. Eurytoma larvae are usually solitary idiobiont ectoparasitoids of the host larva or of larvae of cynipid inquilines that also often feed on gall tissue.