Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts.

This is the final version of the article. Available from the publisher via the DOI in this record.BACKGROUND: Biological invasions provide a window on the process of community assembly. In particular, tracking natural enemy recruitment to invading hosts can reveal the relative roles of co-evolution (including local adaptation) and ecological sorting. We use molecular data to examine colonisation of northern Europe by the parasitoid Megastigmus stigmatizans following invasions of its herbivorous oak gallwasp hosts from the Balkans. Local host adaptation predicts that invading gallwasp populations will have been tracked primarily by sympatric Balkan populations of M. stigmatizans (Host Pursuit Hypothesis). Alternatively, ecological sorting allows parasitoid recruitment from geographically distinct populations with no recent experience of the invading hosts (Host Shift Hypothesis). Finally, we test for long-term persistence of parasitoids introduced via human trade of their hosts' galls (Introduction Hypothesis). RESULTS: Polymorphism diagnostic of different southern refugial regions was present in both mitochondrial and nuclear microsatellite markers, allowing us to identify the origins of northern European invaded range M. stigmatizans populations. As with their hosts, some invaded range populations showed genetic variation diagnostic of Balkan sources, supporting the Host Pursuit Hypothesis. In contrast, other invading populations had an Iberian origin, unlike their hosts in northern Europe, supporting the Host Shift Hypothesis. Finally, both British and Italian M. stigmatizans populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources. CONCLUSIONS: These data reveal the continental scale of multi-trophic impacts of anthropogenic disturbance and highlight the fact that herbivores and their natural enemies may face very different constraints on range expansion. The ability of natural enemies to exploit ecologically-similar hosts with which they have had no historical association supports a major role for ecological sorting processes in the recent assembly of these communities. The multitude of origins of invading natural enemy populations in this study emphasises the diversity of mechanisms requiring consideration when predicting consequences of other biological invasions or biological control introductions.Funding was provided by NERC grant NE/B504406/1 to GNS and KS and NE/E014453/1 to GNS and JAN

Phylogenetic and non-phylogenetic structure in trophic links between gall-forming herbivores and their parasitoid natural enemies.

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 are predictable using models that incorporate phylogenies in place of trait data. We analysed variation in link richness, frequency, and identity in a multi-site dataset of interactions between host oak cynipid galls and parasitoid natural enemies, using a Bayesian mixed modelling framework allowing concurrent fitting of terms for phylogenies of both trophic levels. In both link incidence (presence/absence) and link frequency datasets, we identified strong signatures of cophylogeny (related parasitoids attack related host galls) and patterns independent of either phylogeny. Our results are robust to simulations of substantially reduced sample completeness, and are consistent with the structuring of trophic interactions by a combination of phylogenetically conserved and convergently evolving traits at both trophic levels. We discuss our results in light of phenotypic traits thought to structure gall-parasitoid interactions and wider applications of this approach, including inference of underlying community assembly processes and prediction of economically important trophic interactions

Phylogenetic and non-phylogenetic structure in trophic links between gall-forming herbivores and their parasitoid natural enemies.

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 are predictable using models that incorporate phylogenies in place of trait data. We analysed variation in link richness, frequency, and identity in a multi-site dataset of interactions between host oak cynipid galls and parasitoid natural enemies, using a Bayesian mixed modelling framework allowing concurrent fitting of terms for phylogenies of both trophic levels. In both link incidence (presence/absence) and link frequency datasets, we identified strong signatures of cophylogeny (related parasitoids attack related host galls) and patterns independent of either phylogeny. Our results are robust to simulations of substantially reduced sample completeness, and are consistent with the structuring of trophic interactions by a combination of phylogenetically conserved and convergently evolving traits at both trophic levels. We discuss our results in light of phenotypic traits thought to structure gall-parasitoid interactions and wider applications of this approach, including inference of underlying community assembly processes and prediction of economically important trophic interactions

Environmental factors and host genetic variation shape the fungal endophyte communities within needles of Scots pine (Pinus sylvestris)

To determine the role of environmental and host genetic factors in shaping fungal endophyte communities we used culturing and metabarcoding techniques to quantify fungal taxa within healthy Scots pine (Pinus sylvestris) needles in a 7-y old provenance-progeny trial replicated at three sites. Both methods revealed a community of ascomycete and basidiomycete taxa dominated by the needle pathogen Lophodermium seditiosum. Differences in fungal endophyte taxon composition and diversity indices were highly significant among trial sites. Within two sites, fungal endophyte communities varied significantly among provenances. Furthermore, the communities differed significantly among maternal families within provenances in 11/15 and 7/15 comparisons involving culture and metabarcoding data respectively. We conclude that both environmental and host genetic variation shape the fungal endophyte community of P. sylvestris needles

Evolution of host-plant associations and biogeographic patterns on a global scale within the oak gall wasps

Co-evolutionary interactions between insect herbivores and their host plants underlie much contemporary biodiversity and are vital to assembly of natural ecosystems. Assemblages of galls on oaks induced by Cynipini wasps (Hymenoptera: Cynipidae) occur across much of the Northern Hemisphere, their diversity peaking in the Nearctic and on white oaks (Quercus section Quercus). However, the evolutionary history of the clade has been debated with respect to geographic origins, direction and timings of dispersal events, and shifts in host plant associations. We examined these questions using a global-scale, 6-gene phylogeny of 430 Cynipini species and a dataset of their associated host plants encompassing all eight sections within Quercus plus five Fagaceae genera. Likelihood-based ancestral state reconstructions demonstrate a Nearctic origin of the Cynipini followed by repeated colonisations of the Palearctic via both westwards and eastwards dispersal. These inferences are robust to bias in taxon sampling across continents and the inclusion of Protobalandricus as the sister lineage to Cynipini sensu stricto. Likewise, the association with white oaks is probably ancestral and has been retained by many Cynipini lineages. However, host shifts to other sections within Quercus and related Fagaceae genera are widely distributed across the cynipid phylogeny. They are associated with both global-scale range shifts and within-bioregion exploitation of alternative hosts, and their frequency typically correlates with host-plant relatedness. These findings highlight the evolutionary success of cynipids on white oak hosts and the connectedness of continental assemblages of gall wasps over evolutionary time

Multiple host use and the dynamics of host switching in host–parasite systems

1. The link between multi-host use and host switching in host–parasite interactions is a continuing area of debate. Lycaenid butterflies in the genus Maculinea, for example, exploit societies of different Myrmica ant species across their ranges, but there is only rare evidence that they simultaneously utilise multiple hosts at a local site, even where alternative hosts are present. 2. We present a simple population-genetic model accounting for the proportion of two alternative hosts and the fitness of parasite genotypes on each host. In agreement with standard models, we conclude that simultaneous host use is possible whenever fitness of heterozygotes on alternative hosts is not too low. 3. We specifically focus on host-shifting dynamics when the frequency of hosts changes. We find that (i) host shifting may proceed so rapidly that multiple host use is unlikely to be observed, (ii) back and forth transition in host use can exhibit a hysteresis loop, (iii) the parasites’ host use may not be proportional to local host frequencies and be restricted to the rarer host under some conditions, and (iv) that a substantial decline in parasite abundance may typically precede a shift in host use. 4. We conclude that focusing not just on possible equilibrium conditions but also considering the dynamics of host shifting in non-equilibrium situations may provide added insights into host–parasite systems

Species Accumulation Curves and Incidence-Based Species Richness Estimators to Appraise the Diversity of Cultivable Yeasts from Beech Forest Soils

Background: Yeast-like fungi inhabit soils throughout all climatic zones in a great abundance. While recent estimations predicted a plethora of prokaryotic taxa in one gram of soil, similar data are lacking for fungi, especially yeasts. Methodology/Principal Findings: We assessed the diversity of soil yeasts in different forests of central Germany using cultivation-based techniques with subsequent identification based on rDNA sequence data. Based on experiments using various pre-cultivation sample treatment and different cultivation media we obtained the highest number of yeasts by analysing mixed soil samples with a single nutrient-rich medium. Additionally, several species richness estimators were applied to incidence-based data of 165 samples. All of them predicted a similar range of yeast diversity, namely 14 to 16 species. Randomized species richness curves reached saturation in all applied estimators, thus indicating that the majority of species is detected after approximately 30 to 50 samples analysed. Conclusions/Significance: In this study we demonstrate that robust species identification as well as mathematical approaches are essential to reliably estimate the sampling effort needed to describe soil yeast communities. This approach has great potential for optimisation of cultivation techniques and allows high throughput analysis in the future