Does genomic variation in a foundation species predict arthropod community structure in a riparian forest?

Understanding how genetic variation within a foundation species determines the structure of associated communities and ecosystem processes has been an emerging frontier in ecology. Previous studies in common gardens identified close links between intraspecific variation and multispecies community structure, and these findings are now being evaluated directly in the complex natural ecosystem. In this study, we examined to what extent genomic variation in a foundation tree species explains the structure of associated arthropod communities in the field, comparing with spatial, temporal and environmental factors. In a continuous mixed forest, arthropods were surveyed on 85 mature alders (Alnus hirsuta) in 2 years. Moreover, we estimated Nei's genetic distance among the alders based on 1,077 single nucleotide polymorphisms obtained from restricted-site-associated DNA sequencing of the alders' genome. In both years, we detected significant correlations between genetic distance and dissimilarity of arthropod communities. A generalized dissimilarity modelling indicated that the genetic distance of alder populations was the most important predictor to explain the variance of arthropod communities. Among arthropod functional groups, carnivores were consistently correlated with genetic distance of the foundation species in both years. Furthermore, the extent of year-to-year changes in arthropod communities was more similar between more genetically closed alder populations. This study demonstrates that the genetic similarity rule would be primarily prominent in community assembly of plant-associated arthropods under temporally and spatially variable environments in the field.

Herbivore community promotes trait evolution in a leaf beetle via induced plant response.

Several recent studies have emphasised that community composition alters species trait evolution. Here, we demonstrate that differences in composition of local herbivore communities lead to divergent trait evolution of the leaf beetle Plagiodera versicolora through plant-mediated indirect interactions. Our field surveys, genetic analyses and community-manipulation experiments show that herbivore community composition determines the degree of herbivore-induced regrowth of willows (Salicaceae), which in turn, promotes the divergent evolution of feeding preference in the leaf beetle from exclusive preference for new leaves to a lack of preference among leaf-age types. Regrowth intensity depends both on the differential response of willows to different herbivore species and the integration of those herbivore species in the community. Because herbivore-induced regrowth involves phenological changes in new leaf production, leaf beetle populations develop divergent feeding preferences according to local regrowth intensity. Therefore, herbivore community composition shapes the selection regime for leaf beetle evolution through trait-mediated indirect interactions.

A large-scale field experiment of artificially caused landslides with replications revealed the response of the ground-dwelling beetle community to landslides.

Precipitation-induced landslides, which are predicted to increase under the changing climate, may have large impacts on insect community properties. However, understanding of how insect community properties shift following landslides remains limited because replicated research involving landslides, which are large-scale disturbances with stochastic natural causes, is difficult. To tackle this issue, we conducted a large-scale field experiment by artificially causing landslides at multiple sites. We established 12 landslide sites, each 35 m × 35 m, and 6 undisturbed sites in both planted and natural forests and collected ground-dwelling beetles 1 year later. We found that forest type (i.e., pre-disturbance vegetation) did not affect the structure of a ground-dwelling beetle community disturbed by a landslide (landslide community), but the structure of an undisturbed community was affected by forest type. Moreover, the structures of landslide and undisturbed communities were completely different, possibly because landslides create harsh environments that act as an ecological filter. Thus, a niche-selection process may have a critical role in community assembly at landslide sites. There were no significant differences in species diversity between undisturbed and landslide communities, suggesting that landslides to not reduce species richness overall. However, among-site variability in species composition was much greater at landslide sites than at undisturbed sites. This result suggests that stochastic colonization predominated at the landslide sites more than undisturbed sites. Synthesis and applications. Overall, our results suggest that both deterministic and stochastic processes are critical in community assembly, at least in the early post-landslide stage. Our large-scale manipulative field experiment with replications has thus resulted in new insights into biological community properties after a landslide.

Plant genotypic diversity increases population size of a herbivorous insect.

It is critical to incorporate the process of population dynamics into community genetics studies to identify the mechanisms of the linkage between host plant genetics and associated communities. We studied the effects of plant genotypic diversity of tall goldenrod Solidago altissima on the population dynamics of the aphid Uroleucon nigrotuberculatum. We found genotypic variation in plant resistance to the aphid in our experiments. To determine the impact of plant genotypic diversity on aphid population dynamics, we compared aphid densities under conditions of three treatments: single-genotype plots, mixed-genotype plots and mixed-genotype-with-cages plots. In the latter treatment plants were individually caged to prevent natural enemy attack and aphid movement among plants. The synergistic effects of genotypes on population size were demonstrated by the greater aphid population size in the mixed-genotype treatment than expected from additive effects alone. Two non-exclusive hypotheses are proposed to explain this pattern. First, there is a source-sink relationship among plant genotypes: aphids move from plant genotypes where their reproduction is high to genotypes where their reproduction is low. Second, natural enemy mortality is reduced in mixed plots in a matrix of diverse plant genotypes.

Environmentally triggered variability in the genetic variance-covariance of herbivory resistance of an exotic plant Solidago altissima.

The variability in the genetic variance-covariance (G-matrix) in plant resistance and its role in the evolution of invasive plants have been long overlooked. We conducted an additional analysis of the data of a reciprocal transplant experiment with tall goldenrod, Solidago altissima, in multiple garden sites within its native range (USA) and introduced range (Japan). We explored the differences in G-matrix of resistance to two types of foliar herbivores: (a) a lace bug that is native to the USA and recently introduced to Japan, (b) and other herbivorous insects in response to plant origins and environments. A negative genetic covariance was found between plant resistances to lace bugs and other herbivorous insects, in all combinations of garden locations and plant origins except for US plants planted in US gardens. The G-matrix of the resistance indices did not differ between US and Japanese plants either in US or Japanese gardens, while it differed between US and Japanese gardens in both US and Japanese plants. Our results suggested that the G-matrix of the plant resistance may have changed in response to novel environmental differences including herbivore communities and/or other biotic and abiotic factors in the introduced range. This may have revealed a hidden trade-off between resistances, masked by the environmental factors in the origin range. These results suggest that the stability of the genetic covariance during invasion, and the environmentally triggered variability in the G-matrices of plant resistance may help to protect the plant against multiple herbivore species without changing its genetic architecture and that this may lead to a rapid adaptation of resistance in exotic plants. Local environments of the plant also have a critical effect on plant resistance and should be considered in order to understand trait evolution in exotic plants.

Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant.

Much attention has been paid to ecology and evolution of damage-induced plant responses. Recently, it has been emphasized that phenotypic plasticity, such as induced plant responses, has the potential to lead to evolutionary changes of interacting partners. Here, we report that induced plant regrowth promotes a locally adaptive feeding preference of a leaf beetle, Plagiodera versicolora. We found that there was among-population variation in the strength of the feeding preference of the leaf beetle for leaf-age types of conspecific host plants. The strength of the preference was positively correlated to leaf production of host plants across populations, and the intensity of induced regrowth was likely to have been responsible for geographic variation in new leaf production. Within one population, we detected a significant additive genetic variance and heritability in the preference for consuming new vs. old leaves. Moreover, the strength of preference was significantly related to egg production depending on the leaf-age types. Thus, allopatric populations can evolutionarily develop different adaptive preference, according to locally distinct patterns of induced host regrowth.

Community consequences of herbivore-induced bottom-up trophic cascades: the importance of resource heterogeneity.

1. Herbivory often changes resource quality for herbivorous insects through induced plant responses depending on the intensity of damage. We hypothesized that the willow's response following herbivory affects the entire arthropod community structure on the tree due to changes in plant quality. To examine this hypothesis, we investigated arthropod communities on three willow species, Salix gilgiana, Salix eriocarpa and Salix serissaefolia. 2. In our common garden, cuttings were established in 2003 and experimental treatments were applied in 2005. Damage by a boring caterpillar of a swift moth (Endoclita excrescens) and artificial cutting of 25% stems were applied as partial herbivory within individual trees, and 100% cutting of stems was applied to represent severe herbivory to whole individual trees. These treatments stimulated lateral shoot production depending on damage intensity, resulting in full compensation for biomass loss. 3. Positive relationships were detected between within-tree variation in foliar nitrogen content and overall abundance/species richness of herbivores. Moth boring and 25% cutting increased herbivore abundance and species richness relative to controls. However, we found no significant differences in herbivore abundance and species richness between 100% cut and control trees. Community composition of herbivore species was significantly different between the following three groups: (i) bored and 25% cut; (ii) 100% cut; and (iii) control trees. Changes in community structure of herbivores were likely due to changes in plant quality depending on the intensity of damage. 4. Although total predator abundance and species richness were not significantly different among treatments, community composition of predator species was significantly different among treatments. 5. These results indicate that herbivore-induced willow responses can largely determine the entire arthropod community structure of multitrophic levels due to changes in plant quality. We suggest that heterogeneous resource conditions induced by herbivory within and among plant individuals increase the species diversity of arthropods.