Putting the genes into community genetics

As part of the long‐term fusion of evolutionary biology and ecology (Ford, 1964), the field of community genetics has made tremendous progress in describing the impacts of plant genetic variation on community and ecosystem processes. In the “genes‐to‐ecosystems” framework (Whitham et al., 2003), genetically based traits of plant species have ecological consequences, but previous studies have not identified specific plant genes responsible for community phenotypes. The study by Barker et al. (2019) in this issue of Molecular Ecology uses an impressive common garden experiment of trembling aspen (Figure 1) to test for the genetic basis of tree traits that shape the insect community composition. Using a Genome‐Wide Association Study (GWAS), they found that genomic regions associated with phytochemical traits best explain variation in herbivore community composition, and identified specific genes associated with different types of leaf‐modifying herbivores and ants. This is one of the first studies to identify candidate genes underlying the heritable plant traits that explain patterns of insect biodiversity.     

Spatial soil heterogeneity has a greater effect on symbiotic arbuscular mycorrhizal fungal communities and plant growth than genetic modification with Bacillus thuringiensis toxin genes

Maize, genetically modified with the insect toxin genes of Bacillus thuringiensis (Bt), is widely cultivated, yet its impacts on soil organisms are poorly understood. Arbuscular mycorrhizal fungi (AMF) form symbiotic associations with plant roots and may be uniquely sensitive to genetic changes within a plant host. In this field study, the effects of nine different lines of Bt maize and their corresponding non‐Bt parental isolines were evaluated on AMF colonization and community diversity in plant roots. Plants were harvested 60 days after sowing, and data were collected on plant growth and per cent AMF colonization of roots. AMF community composition in roots was assessed using 454 pyrosequencing of the 28S rRNA genes, and spatial variation in mycorrhizal communities within replicated experimental field plots was examined. Growth responses, per cent AMF colonization of roots and AMF community diversity in roots did not differ between Bt and non‐Bt maize, but root and shoot biomass and per cent colonization by arbuscules varied by maize cultivar. Plot identity had the most significant effect on plant growth, AMF colonization and AMF community composition in roots, indicating spatial heterogeneity in the field. Mycorrhizal fungal communities in maize roots were autocorrelated within approximately 1 m, but at greater distances, AMF community composition of roots differed between plants. Our findings indicate that spatial variation and heterogeneity in the field has a greater effect on the structure of AMF communities than host plant cultivar or modification by Bt toxin genes.     

Intraspecific variation in host plant traits mediates taxonomic and functional composition of local insect herbivore communities

1. Host plant phenotypic traits affect the structure of the associated consumer community and mediate species interactions. Intraspecific variation in host traits is well documented, although a functional understanding of variable traits that drive herbivore community response is lacking. We address this gap by modelling the trait-environment relationship using insect traits and host plant traits in a multilevel model. 2. We compare herbivore assemblages from the canopy of the phenotypically variable tree Metrosideros polymorpha on Hawai‘i Island. Multiple distinct varieties of M. polymorpha frequently co-occur, with variation in morphological traits. Using this system, we identify host and insect traits that underlie patterns of herbivore abundance and quantify the strength of host-insect trait interactions. 3. This work examines plant-insect interactions at a community scale, across 36 herbivore species in three orders. We find that co-occurring trees of varying phenotype support distinct communities. Leaf traits, including specific leaf area, trichome presence, and leaf nutrients, explain 46% of variation in insect communities. We find that feeding guild and nymphal life history are correlated with host plant traits, and we show that model predictions are improved by including the host and insect trait interaction. 4. This study demonstrates how insect herbivores traits influence community response to morphologically variable hosts. Environmental heterogeneity indirectly affected herbivore community structure via intraspecific variation in host plants, providing an important source of variation for maintaining diversity in the broader community.     

Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage

Intraspecific plant diversity can modify the properties of associated arthropod communities and plant fitness. However, it is not well understood which plant traits determine these ecological effects. We explored the effect of intraspecific chemical diversity among neighbouring plants on the associated invertebrate community and plant traits. In a common garden experiment, intraspecific diversity among neighbouring plants was manipulated using three plant populations of wild cabbage that differ in foliar glucosinolates. Plants were larger, harboured more herbivores, but were less damaged when plant diversity was increased. Glucosinolate concentration differentially correlated with generalist and specialist herbivore abundance. Glucosinolate composition correlated with plant damage, while in polycultures, variation in glucosinolate concentrations among neighbouring plants correlated positively with herbivore diversity and negatively with plant damage levels. The results suggest that intraspecific variation in secondary chemistry among neighbouring plants is important in determining the structure of the associated insect community and positively affects plant performance.     

Strong associations between plant genotypes and bacterial communities in a natural salt marsh

Although microbial communities have been shown to vary among plant genotypes in a number of experiments in terrestrial ecosystems, relatively little is known about this relationship under natural conditions and outside of select model systems. We reasoned that a salt marsh ecosystem, which is characterized by twice‐daily flooding by tides, would serve as a particularly conservative test of the strength of plant–microbial associations, given the high degree of abiotic regulation of microbial community assembly resulting from alternating periods of inundation and exposure. Within a salt marsh in the northeastern United States, we characterized genotypes of the foundational plant Spartina alterniflora using microsatellite markers, and bacterial metagenomes within marsh soil based on pyrosequencing. We found significant differences in bacterial community composition and diversity between bulk and rhizosphere soil, and that the structure of rhizosphere communities varied depending on the growth form of, and genetic variation within, the foundational plant S. alterniflora. Our results indicate that there are strong plant–microbial associations within a natural salt marsh, thereby contributing to a growing body of evidence for a relationship between plant genotypes and microbial communities from terrestrial ecosystems and suggest that principles of community genetics apply to this wetland type.     

The contribution of evening primrose (<Emphasis Type="Italic">Oenothera biennis</Emphasis>) to a modern synthesis of evolutionary ecology

In this review, I consider the contribution that common evening primrose (Oenothera biennis) has made towards integrating the ecology, evolution and genetics of species interactions. Oenothera biennis was among the earliest plant models in genetics and cytogenetics and it played an important role in the modern synthesis of evolutionary biology. More recently, population and ecological genetics approaches have provided insight into the patterns of genetic variation within and between populations, and how a combination of abiotic and biotic factors maintain and select on heritable variation within O. biennis populations. From an ecological perspective, field experiments show that genetic variation and evolution within populations can have cascading effects throughout communities. Plant genotype affects the preference and performance of individual arthropod populations, as well as the composition, biomass, total abundance and diversity of arthropod species on plants. A combination of experiments and simulation models show that natural selection on specific plant traits can drive rapid ecological changes in these same community variables. At the patch level, increasing genotypic diversity leads to a greater abundance and diversity of omnivorous and predaceous arthropods, which is also associated with increased biomass and fecundity of plants in genetically diverse patches. Finally, in questioning whether a community genetics perspective is needed in biology, I review several multifactorial experiments which show that plant genotype often explains as much variation in community variables as other ecological factors typically identified as most important in ecology. As a whole, research in the O. biennis system has contributed to a more complete understanding of the dynamic interplay between ecology, evolution and genetics.     

Disparate effects of plant genotypic diversity on foliage and litter arthropod communities

Intraspecific diversity can influence the structure of associated communities, though whether litter-based and foliage-based arthropod communities respond to intraspecific diversity in similar ways remains unclear. In this study, we compared the effects of host-plant genotype and genotypic diversity of the perennial plant, Solidago altissima, on the arthropod community associated with living plant tissue (foliage-based community) and microarthropods associated with leaf litter (litter-based community). We found that variation among host-plant genotypes had strong effects on the diversity and composition of foliage-based arthropods, but only weak effects on litter-based microarthropods. Furthermore, host-plant genotypic diversity was positively related to the abundance and diversity of foliage-based arthropods, and within the herbivore and predator trophic levels. In contrast, there were minimal effects of plant genotypic diversity on litter-based microarthropods in any trophic level. Our study illustrates that incorporating communities associated with living foliage and senesced litter into studies of community genetics can lead to very different conclusions about the importance of intraspecific diversity than when only foliage-based community responses are considered in isolation. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure

Contemporary insights from evolutionary ecology suggest that population divergence in ecologically important traits within predators can generate diversifying ecological selection on local community structure. Many studies acknowledging these effects of intraspecific variation assume that local populations are situated in communities that are unconnected to similar communities within a shared region. Recent work from metacommunity ecology suggests that species dispersal among communities can also influence species diversity and composition but can depend upon the relative importance of the local environment. Here, we study the relative effects of intraspecific phenotypic variation in a fish predator and spatial processes related to plankton species dispersal on multitrophic lake plankton metacommunity structure. Intraspecific diversification in foraging traits and residence time of the planktivorous fish alewife (Alosa pseudoharengus) among coastal lakes yields lake metacommunities supporting three lake types which differ in the phenotype and incidence of alewife: lakes with anadromous, landlocked, or no alewives. In coastal lakes, plankton community composition was attributed to dispersal versus local environmental predictors, including intraspecific variation in alewives. Local and beta diversity of zooplankton and phytoplankton was additionally measured in response to intraspecific variation in alewives. Zooplankton communities were structured by species sorting, with a strong influence of intraspecific variation in A. pseudoharengus. Intraspecific variation altered zooplankton species richness and beta diversity, where lake communities with landlocked alewives exhibited intermediate richness between lakes with anadromous alewives and without alewives, and greater community similarity. Phytoplankton diversity, in contrast, was highest in lakes with landlocked alewives. The results indicate that plankton dispersal in the region supplied a migrant pool that was strongly structured by intraspecific variation in alewives. This is one of the first studies to demonstrate that intraspecific phenotypic variation in a predator can maintain contrasting patterns of multitrophic diversity in metacommunities.     

Abiotic drivers and plant traits explain landscape‐scale patterns in soil microbial communities

The controls on aboveground community composition and diversity have been extensively studied, but our understanding of the drivers of belowground microbial communities is relatively lacking, despite their importance for ecosystem functioning. In this study, we fitted statistical models to explain landscape‐scale variation in soil microbial community composition using data from 180 sites covering a broad range of grassland types, soil and climatic conditions in England. We found that variation in soil microbial communities was explained by abiotic factors like climate, pH and soil properties. Biotic factors, namely community‐weighted means (CWM) of plant functional traits, also explained variation in soil microbial communities. In particular, more bacterial‐dominated microbial communities were associated with exploitative plant traits versus fungal‐dominated communities with resource‐conservative traits, showing that plant functional traits and soil microbial communities are closely related at the landscape scale.     

Diversity protects plant communities against generalist molluscan herbivores

Wildflower strips are used to increase natural enemies of crop pests and to conserve insect diversity on farmland. Mollusks, especially slugs, can affect the vegetation development in these strips considerably. Although recent theoretical work suggests that more diverse plant communities will exhibit greater resistance against herbivore pressure, empirical studies are scarce. We conducted a semi‐natural experiment in wildflower strips, manipulating trophic structure (reduction in herbivorous mollusks and reduction in major predators) and plant diversity (2, 6, 12, 20 and 24 sown species). This design allowed us to assess the effect of plant diversity, biomass and composition on mollusks, and vice versa, the effect of mollusc abundance on vegetation. Seven species of mollusks were found in the strips, with the slugs Arion lusitanicus, Deroceras reticulatum and Deroceras panormitanum being most frequent. We found a negative relationship between plant diversity and mollusk abundance, which was due predominantly to a decrease in the agricultural pest species A. lusitanicus. These results are consistent with the hypothesis that plant diversity can reduce the impact of herbivores. However, plant identity also had an effect on mollusks, and accounted for a much larger fraction of the variation in mollusk communities than biodiversity effects. While overall plant diversity decreased during the 3 years of the study, in the final year the highest plant diversity was found in the plots where mollusk populations were experimentally reduced. We conclude that selective feeding by generalist herbivores leads to changes in plant community composition and hence reduced plant diversity. Our results highlight the importance of plant biodiversity as protection against generalist herbivores, which if abundant can in the long term negatively impact plant diversity, driving the system along a “low plant diversity – high mollusk abundance” trajectory.     

The influence of range‐wide plant genetic variation on soil invertebrate communities

Plant genetic variation can have far‐reaching effects on associated communities and ecosystems. Heritable variation in ecologically relevant plant traits is often non‐randomly distributed across a species’ range and can exhibit geographic clines. In the event of range expansions and migration, previously unfamiliar genotypes may have large impacts on resident communities and ecosystems due to the introduction of novel and heritable phenotypic variation. Here we test the hypothesis that geographic origin of a focal plant genotype has effects on belowground invertebrate communities using a common garden field experiment. We sampled soil invertebrates from 103 Oenothera biennis genotypes, which were collected from across the species’ range and planted into a common garden field experiment at the northern range limit. We enumerated 24 000 individuals from 190 morphospecies and found that the diversity, abundance, and composition of soil invertebrate communities varied greatly among plant genotypes. Despite strong effects of plant genotype, we found few genetic correlations between plant traits and soil invertebrate community variables. However, herbivore damage was strongly related to variation in the soil invertebrate community. Geographic origin of plant genotypes had at most a weak effect on belowground communities. We speculate that predicting the extended effects of population movement on associated communities will require detailed knowledge of the trait variation occurring within focal species across particular environmental gradients.     

A quantitative genetic approach for predicting ecological change in biological communities

Ecological studies of communities have become increasingly focused on the role of genetics. These studies often conclude that genetics and evolution play an important role in community structure and function. For instance, studies have shown that the structure of insect communities associated with a host plant is heritable and therefore can potentially evolve. However, when studying communities of interacting species two problems are faced: (1) the traits that determine the outcomes of these interactions are often unknown, and (2) communities are normally highly multidimensional (n-dimensional for n species). In order to surmount these problems, we adapt a commonly used approach for studying the evolution of multivariate quantitative traits to the study of biological communities. Specifically, we propose utilizing a community-based genetic covariance matrix (G-matrix) and an associated vector of community selection gradients for predicting changes in community composition, where the “traits” under study are the abundances, or other properties, of various interacting species. This approach capitalizes on the relative ease with which data on the abundance of individuals interacting with individuals of a focal species (e.g., abundances of various herbivorous insects on a plant) can be collected and on the utility of the quantitative genetic approach for predicting multidimensional evolution. In order to evaluate the utility and accuracy of the G-matrix approach for predicting the evolution of communities, we develop and analyze numerical simulations of evolving communities. Results of these simulations show that an approach based on community G-matrices and selection gradients provides a rich understanding of how underlying genetics shape community structure and, in many cases, accurately predicts how community structure changes over time.     

Impacts of climate warming on hybrid zone movement: Geographically diffuse and biologically porous “species borders”

Abstract The ecology and evolutionary biology of insect–plant associations has realized extensive attention, especially during the past 60 years. The classifications (categorical designations) of continuous variation in biodiversity, ranging from global patterns (e.g., latitudinal gradients in species richness/diversity and degree of herbivore feeding specialization) to localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious. Semantic and biosystematic (taxonomical) disagreements sometimes detract from more important ecological and evolutionary processes that drive diversification, the dynamics of gene flow and local extinctions. This review addresses several aspects of insect specialization, host‐associated divergence and ecological (including “hybrid”) speciation, with special reference to the climate warming impacts on species borders of hybridizing swallowtail butterflies (Papilionidae). Interspecific hybrid introgression may result in collapse of multi‐species communities or increase species numbers via homoploid hybrid speciation. We may see diverging, merging, or emerging genotypes across hybrid zones, all part of the ongoing processes of evolution. Molecular analyses of genetic mosaics and genomic dynamics with “divergence hitchhiking”, combined with ecological, ethological and physiological studies of “species porosity”, have already begun to unveil some answers for some important ecological/evolutionary questions. (i) How rapidly can host‐associated divergence lead to new species (and why doesn't it always do so, e.g., resulting in “incomplete” speciation)? (ii) How might “speciation genes” function, and how/where would we find them? (iii) Can oscillations from specialists to generalists and back to specialists help explain global diversity in herbivorous insects? (iv) How could recombinant interspecific hybridization lead to divergence and speciation? From ancient phytochemically defined angiosperm affiliations to recent and very local geographical mosaics, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of ecological patterns and evolutionary processes, including host‐associated genetic divergence, genomic mosaics, genetic hitchhiking and sex‐linked speciation genes. Apparent homoploid hybrid speciation in Papilio appears to have been catalyzed by climate warming‐induced interspecific introgression of some, but not all, species diagnostic traits, reflecting strong divergent selection (discordant), especially on the Z (= X) chromosome. Reproductive isolation of these novel recombinant hybrid genotypes appears to be accomplished via a delayed post‐diapause emergence or temporal isolation, and is perhaps aided by the thermal landscape. Changing thermal landscapes appear to have created (and may destroy) novel recombinant hybrid genotypes and hybrid species.     

Community structure and abundance of insects in response to early‐season aphid infestation in wild cabbage populations

1. Changes in the arthropod community structure can be attributed to differences in constitutively expressed plant traits or those that change depending on environmental conditions such as herbivory. Early‐season herbivory may have community‐wide effects on successive insect colonisation of host plants and the identity of the initially inducing insect may determine the direction and strength of the effects on the dynamics and composition of the associated insect community. 2. Previous studies have addressed the effect of early infestation with a chewing herbivore. In the present study, the effect of early infestation was investigated with a phloem‐feeding aphid [Brevicoryne brassicae L. (Hemiptera, Aphididae)] on the insect community associated with three wild cabbage (Brassica oleracea L.) populations, which are known to differ in defence chemistry, throughout the season in field experiments. 3. Aphid infestation had asymmetric effects on the associated insect community and only influenced the abundance of the natural enemies of aphids, but not that of chewing herbivores and their natural enemies. The effect size of aphid infestation further depended on the cabbage population. 4. Aphid feeding has been previously reported to promote host‐plant quality for chewing herbivores, which has been attributed to antagonism between the two major defence signalling pathways controlled by the hormones salicylic acid (SA) and jasmonic acid (JA), respectively. Our results show no effects of early infestation by aphids on chewing herbivores, suggesting the absence of long‐term JA–SA antagonism. 5. Investigating the effects of the identity of an early‐season coloniser and genotypic variation among plant populations on insect community dynamics are important in understanding insect–plant community ecology.     

Soil nutrients trump intraspecific effects on understory plant communities

Understanding the links between intraspecific genetic variation and patterns of diversity in associated communities has been the primary focus of community genetics or ‘genes-to-ecosystem’ research in ecology. While other ecological factors, such as the abiotic environment, have well-documented influences on communities, the relative contributions of genetic variation versus the environment to species interactions remains poorly explored. In this study, we use a common garden experiment to study a coastal dune plant community dominated by the shrub, Baccharis pilularis, which displays a morphological dimorphism in plant architecture. We found the differences in the understory plant community between erect and prostrate morphs of Baccharis to be statistically significant, but small relative to the impacts of nutrient additions (NPK and C additions), for the richness, cover, and biomass of the understory plant community. There were no significant interactions between Baccharis morphology and nutrient-addition treatments, suggesting the influence of nutrient addition was consistent between erect and prostrate morphs. Moreover, we found no difference in overall plant community composition between Baccharis morphs, while NPK additions led to shifts in understory community composition compared to unfertilized shrubs. In sum, our results indicate that nutrients are the more important factor governing understory plant community structure in a coastal dunes ecosystem followed by intraspecific variation in dominant shrub architecture. Our results address a growing call to understand the extended consequences of intraspecific variation across heterogeneous environments in terrestrial ecosystems.     

Consequences of variation in plant defense for biodiversity at higher trophic levels

Antagonistic interactions between insect herbivores and plants impose selection on plants to defend themselves against these attackers. Although selection on plant defense traits has typically been studied for pairwise plant-attacker interactions, other community members of plant-based food webs are unavoidably affected by these traits as well. A plant trait might, for example, affect parasitoids and predators feeding on the herbivore. Consequently, defensive plant traits structure the diversity and composition of the complex community associated with the plant, and communities as a whole also feed back to selection on plant traits. Here, we review recent developments in our understanding of how plant defense traits structure insect communities and discuss how molecular mechanisms might drive community-wide effects.     

Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses

It is increasingly recognized that the ecology of communities and evolution of species within communities are interdependent, and researchers have been paying attention to this rapidly emerging field of research, i.e., through studies on eco-evolutionary dynamics. Most of the studies on eco-evolutionary dynamics have been concerned with direct trophic interactions. However, community ecologists have shown that trait-mediated indirect effects play an important role in shaping the structure of natural communities. In particular, in terrestrial plant–insect systems, indirect effects mediated through herbivore-induced plant responses are common and have a great impact on the structure of herbivore communities. This review describes eco-evolutionary dynamics in herbivorous insect communities, and specifically focuses on the key role of herbivore-induced plant responses in eco-evolutionary dynamics. First, I review studies on the evolution of herbivore traits relevant to plant induction and discuss evolution in a community context mediated by induced plant responses. Second, I highlight how intraspecific genetic variation or evolution in herbivore traits can influence herbivore community structure. Finally, I propose the hypothetical model that induced plant responses supports eco-evolutionary feedback in herbivore communities. In this review, I argue that the application of the indirect interaction web approaches into studies on eco-evolutionary will provide profound insights into understanding of mechanisms of the generation and maintenance of biodiversity.     

Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie

Symbiotic associations between plants and arbuscular mycorrhizal (AM) fungi are ubiquitous in many herbaceous plant communities and can have large effects on these communities and ecosystem processes. The extent of species-specificity between these plant and fungal symbionts in nature is poorly known, yet reciprocal effects of the composition of plant and soil microbe communities is an important assumption of recent theoretical models of plant community structure. In grassland ecosystems, host plant species may have an important role in determining development and sporulation of AM fungi and patterns of fungal species composition and diversity. In this study, the effects of five different host plant species [Poa pratensis L., Sporobolus heterolepis (A. Gray) A. Gray, Panicum virgatum L., Baptisia bracteata Muhl. ex Ell., Solidago missouriensis Nutt.] on spore communities of AM fungi in tallgrass prairie were examined. Spore abundances and species composition of fungal communities of soil samples collected from patches within tallgrass prairie were significantly influenced by the host plant species that dominated the patch. The AM fungal spore community associated with B. bracteata showed the highest species diversity and the fungi associated with Pa. virgatum showed the lowest diversity. Results from sorghum trap cultures using soil collected from under different host plant species showed differential sporulations of AM fungal species. In addition, a greenhouse study was conducted in which different host plant species were grown in similar tallgrass prairie soil. After 4 months of growth, AM fungal species composition was significantly different beneath each host species. These results strongly suggest that AM fungi show some degree of host-specificity and are not randomly distributed in tallgrass prairie. The demonstration that host plant species composition influences AM fungal species composition provides support for current feedback models predicting strong regulatory effects of soil communities on plant community structure. Differential responses of AM fungi to host plant species may also play an important role in the regulation of species composition and diversity in AM fungal communities. Received: 29 January 1999 / Accepted: 20 October 1999     

Geographic structure in metabolome and herbivore community co‐occurs with genetic structure in plant defence genes

Plant–herbivore interactions vary across the landscape and have been hypothesised to promote local adaption in plants to the prevailing herbivore regime. Herbivores that feed on European aspen (Populus tremula) change across regional scales and selection on host defence genes may thus change at comparable scales. We have previously observed strong population differentiation in a set of inducible defence genes in Swedish P. tremula. Here, we study the geographic patterns of abundance and diversity of herbivorous insects, the untargeted metabolome of the foliage and genetic variation in a set of wound‐induced genes and show that the geographic structure co‐occurs in all three data sets. In response to this structure, we observe local maladaptation of herbivores, with fewer herbivores on local trees than on trees originated from more distant localities. Finally, we also identify 28 significant associations between single nucleotide polymorphisms SNPs from defence genes and a number of the herbivore traits and metabolic profiles.