Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps.

Oak gallwasps (Hymenoptera, Cynipidae, Cynipini) are one of seven major animal taxa that commonly reproduce by cyclical parthenogenesis (CP). A major question in research on CP taxa is the frequency with which lineages lose their sexual generations, and diversify as purely asexual radiations. Most oak gallwasp species are only known from an asexual generation, and secondary loss of sex has been conclusively demonstrated in several species, particularly members of the holarctic genus Andricus. This raises the possibility of widespread secondary loss of sex in the Cynipini, and of diversification within purely parthenogenetic lineages. We use two approaches based on analyses of allele frequency data to test for cryptic sexual generations in eight apparently asexual European species distributed through a major western palaearctic lineage of the gallwasp genus Andricus. All species showing adequate levels of polymorphism (7/8) showed signatures of sex compatible with cyclical parthenogenesis. We also use DNA sequence data to test the hypothesis that ignorance of these sexual generations (despite extensive study on this group) results from failure to discriminate among known but morphologically indistinguishable sexual generations. This hypothesis is supported: 35 sequences attributed by leading cynipid taxonomists to a single sexual adult morphospecies, Andricus burgundus, were found to represent the sexual generations of at least six Andricus species. We confirm cryptic sexual generations in a total of 11 Andricus species, suggesting that secondary loss of sex is rare in Andricus.

The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari.

Human dispersal of organisms is an important process modifying natural patterns of biodiversity. Such dispersal generates new patterns of genetic diversity that overlie natural phylogeographical signatures, allowing discrimination between alternative dispersal mechanisms. Here we use allele frequency and DNA sequence data to distinguish between alternative scenarios (unassisted range expansion and long range introduction) for the colonization of northern Europe by an oak-feeding gallwasp, Andricus kollari. Native to Mediterranean latitudes from Portugal to Iran, this species became established in northern Europe following human introduction of a host plant, the Turkey oak Quercus cerris. Colonization of northern Europe is possible through three alternative routes: (i) unassisted range expansion from natural populations in the Iberian Peninsula; (ii) unassisted range expansion from natural populations in Italy and Hungary; or (iii) descent from populations imported to the UK as trade goods from the eastern Mediterranean in the 1830s. We show that while populations in France were colonized from sources in Italy and Hungary, populations in the UK and neighbouring parts of coastal northern Europe encompass allozyme and sequence variation absent from the known native range. Further, these populations show demographic signatures expected for large stable populations, rather than signatures of rapid population growth from small numbers of founders. The extent and spatial distribution of genetic diversity in the UK suggests that these A. kollari populations are derived from introductions of large numbers of individuals from each of two genetically divergent centres of diversity in the eastern Mediterranean. The strong spatial patterning in genetic diversity observed between different regions of northern Europe, and between sites in the UK, is compatible with leptokurtic models of population establishment.

Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae.

Many studies have addressed the latitudinal gradients in intraspecific genetic diversity of European taxa generated during postglacial range expansion from southern refugia. Although Asia Minor is known to be a centre of diversity for many taxa, relatively few studies have considered its potential role as a Pleistocene refugium or a potential source for more ancient westward range expansion into Europe. Here we address these issues for an oak gallwasp, Andricus quercustozae (Hymenoptera: Cynipidae), whose distribution extends from Morocco along the northern coast of the Mediterranean through Turkey to Iran. We use sequence data for a fragment of the mitochondrial gene cytochrome b and allele frequency data for 12 polymorphic allozyme loci to answer the following questions: (1). which regions represent current centres of genetic diversity for A. quercustozae? Do eastern populations represent one refuge or several discrete glacial refugia? (2). Can we infer the timescale and sequence of the colonization processes linking current centres of diversity? Our results suggest that A. quercustozae was present in five distinct refugia (Iberia, Italy, the Balkans, southwestern Turkey and northeastern Turkey) with recent genetic exchange between Italy and Hungary. Genetic diversity is greatest in the Turkish refugia, suggesting that European populations are either (a). derived from Asia Minor, or (b). subject to more frequent population bottlenecks. Although Iberian populations show the lowest diversity for putatively selectively neutral markers, they have colonized a new oak host and represent a genetically and biologically discrete entity within the species.

Use of population genetic data to infer oviposition behaviour: species-specific patterns in four oak gallwasps (Hymenoptera: Cynipidae).

Many species of oak gallwasp (Hymenoptera: Cynipidae: Cynipini) induce galls containing more than one larva (multilocular galls) on their host plant. To date, it has remained unclear whether multilocular galls result solely from clustered oviposition by a single female, or include the aggregated offspring of several females (multiple founding). We have developed a novel maximum-likelihood approach for use with population genetic data that estimates the number and genotypes of parents contributing to offspring from each gall. We apply this method to allozyme data from multiple populations of four oak gallwasps whose asexual generations develop in multilocular galls (Andricus coriarius, A. lucidus, A. panteli and A. seckendorffi). We find strong evidence for multiple founding in all four species, and show the data to be compatible with multiple founding rather than founding by a single foundress mated with multiple males. The extent of multiple founding differs among species: in A. lucidus and A. seckendorffi most galls are induced by a single female, whereas in A. coriarius and A. panteli over half of the galls sampled were multiple founded. We suggest that variation in levels of multiple founding may be due to consistent ecological differences between the four species.

The population biology of oak gall wasps (Hymenoptera: Cynipidae).

Oak gall wasps (Hymenoptera: Cynipidae, Cynipini) are characterized by possession of complex cyclically parthenogenetic life cycles and the ability to induce a wide diversity of highly complex species- and generation-specific galls on oaks and other Fagaceae. The galls support species-rich, closed communities of inquilines and parasitoids that have become a model system in community ecology. We review recent advances in the ecology of oak cynipids, with particular emphasis on life cycle characteristics and the dynamics of the interactions between host plants, gall wasps, and natural enemies. We assess the importance of gall traits in structuring oak cynipid communities and summarize the evidence for bottom-up and top-down effects across trophic levels. We identify major unanswered questions and suggest approaches for the future.