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

Partitioning of herbivore hosts across time and food plants promotes diversification in the <i>Megastigmus dorsalis</i> oak gall parasitoid complex

Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host-associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host- plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host-associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe

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

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

<p>Abstract</p> <p>Background</p> <p>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 <it>Megastigmus stigmatizans </it>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 <it>M. stigmatizans </it>(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).</p> <p>Results</p> <p>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 <it>M. stigmatizans </it>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 <it>M. stigmatizans </it>populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources.</p> <p>Conclusions</p> <p>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.</p

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