Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Thus far, research has shown that plant genetics can underlie variation in the composition of associated communities (e.g., insects, lichen and endophytes), and those communities can therefore be considered as extended phenotypes. This work, however, has been conducted primarily at the plant genotype level and has not identified the key underlying genes. To address this gap, we used genome‐wide association mapping with a population of 445 aspen (Populus tremuloides) genets to identify the genes governing variation in plant traits (defence chemistry, bud phenology, leaf morphology, growth) and insect community composition. We found 49 significant SNP associations in 13 Populus genes that are correlated with chemical defence compounds and insect community traits. Most notably, we identified an early nodulin‐like protein that was associated with insect community diversity and the abundance of interacting foundation species (ants and aphids). These findings support the concept that particular plant traits are the mechanistic link between plant genes and the composition of associated insect communities. In putting the “genes” into “genes to ecosystems ecology”, this work enhances understanding of the molecular genetic mechanisms that underlie plant–insect associations and the consequences thereof for the structure of ecological communities.
Background and Aims Intraspecific variation in foundation species of forest ecosystems can shape community and ecosystem properties, particularly when that variation has a genetic basis. Traits mediating interactions with other species are predicted by simple allocation models to follow ontogenetic patterns that are rarely studied in trees. The aim of this research was to identify the roles of genotype, ontogeny and genotypic trade-offs shaping growth, defence and reproduction in aspen. Methods We established a common garden replicating >500 aspen genets in Wisconsin, USA. Trees were measured through the juvenile period into the onset of reproduction, for growth, defence chemistry (phenolic glycosides and condensed tannins), nitrogen, extrafloral nectaries, leaf morphology (specific leaf area), flower production and foliar herbivory and disease. We also assayed the TOZ19 sex marker and heterozygosity at ten microsatellite loci. Key Results We found high levels of genotypic variation for all traits, and high heritabilities for both the traits and their ontogenetic trajectories. Ontogeny strongly shaped intraspecific variation, and trade-offs among growth, defence and reproduction supported some predictions while contradicting others. Both direct resistance (chemical defence) and indirect defence (extrafloral nectaries) declined during the juvenile stage, prior to the onset of reproduction. Reproduction was higher in trees that were larger, male and had higher individual heterozygosity. Growth was diminished by genotypic allocation to both direct and indirect defence as well as to reproduction, but we found no evidence of trade-offs between defence and reproduction. Conclusions Key traits affecting the ecological communities of aspen have high levels of genotypic variation and heritability, strong patterns of ontogeny and clear trade-offs among growth, defence and reproduction. The architecture of aspen’s community genetics – its ontogeny, trade-offs and especially its great variability – is shaped by both its broad range and the diverse community of associates, and in turn further fosters that diversity.
Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Multiple studies have shown that different plant genotypes harbor different communities of associated organisms, such as insects. Yet, the mechanistic links that tie insect community composition to plant genetics are still not well understood. To shed light on these relationships, we explored variation in both plant traits (e.g., growth, phenology, defense) and herbivorous insect and ant communities on 328 replicated aspen (Populus tremuloides) genets grown in a common garden. We measured traits and visually surveyed insect communities annually in 2014 and 2015. We found that insect communities overall exhibited low heritability and were shaped primarily by relationships among key insects (i.e., aphids, ants, and free-feeders). Several tree traits affected insect communities and the presence/absence of species and functional groups. Of these traits, tree size and foliar phenology were the most important. Larger trees had denser (i.e., number of insects per unit tree size) and more diverse insect communities, while timing of bud break and bud set differentially influenced particular species and insect groups, especially leaf modifying insects. These findings will inform future research directed toward identification of plant genes and genetic regions that underlie the structure of associated insect communities.
Ecological research has increasingly highlighted the importance of intraspecific variation in shaping the structure and function of communities and ecosystems. Indeed, the effects of intraspecific variation can match or exceed those of interspecific variation. Previous reviews of intraspecific variation in plant traits across heterogeneous environments have focused primarily on mean phenotypic effects. We propose that a richer and fuller understanding of the ecological causes and consequences of intraspecific variation would be provided by partitioning trait variance into its subcomponents (genetic, environment, genotype by environment interaction). We used a meta‐analysis of 352 sets of genetic, environment and genotype by environment (G×E) variation estimates from 72 studies of Salicaceae to compare these sources of variation across plant traits (growth, foliar nitrogen, defence compounds), insect herbivore performance metrics (e.g., survival, growth, fecundity) and environmental conditions (e.g., soil nutrients, water, defoliation). Our findings revealed that variation in levels of defence compounds (both condensed tannins and salicinoids) and insect herbivore performance were primarily genetically determined, while variation in plant growth and foliar nitrogen was more environmentally determined. Plasticity in plant growth, foliar nitrogen levels and insect herbivore performance varied substantially across different sites (year × location), and nutrient, water and carbon dioxide environments. Plasticity was lowest for chemical defence traits and all traits in contrasting ozone and defoliation environments. Our quantitative review also revealed several gaps in the literature, including a need for surveying more mature plants, a wider variety of insect herbivore species (e.g., leaf‐galling insects, specialist insects) and underrepresented environmental treatments (e.g., competition, defoliation, disease, light and water availability). Findings from this analysis highlight the importance of, and patterns within, intraspecific variation with respect to shaping the evolvability and plasticity of traits and governing the interactions of plants and insects. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13249/suppinfo is available for this article.
24Diseases can markedly alter the ecological and economic value of poplars. To better 25 understand poplar-pathogen interactions, we investigated the independent and interactive effects 26 of tree genotype, soil nutrient limitation, and interspecific competition on incidence of powdery 27 mildew (caused by the fungal obligate pathogen Erysiphe adunca) in a foundation tree species, 28 trembling aspen (Populus tremuloides). We established a common garden of potted aspen 29 saplings, incorporating five tree genotypes, two levels of soil nutrients (low and high), and two 30 levels of competition (with and without grass). We then surveyed natural incidence of powdery 31 mildew and aspen vigor (i.e., growth). Incidence of powdery mildew varied among aspen 32 genotypes, and variance in incidence shifted among environments in which the trees were grown. 33Added soil nutrients increased powdery mildew incidence on aspen, whereas grass competition 34 had the opposite effect. Interestingly, grass competition either enhanced or dampened the 35 variance in incidence of powdery mildew among tree genotypes, depending on soil nutrient 36 levels. In addition, powdery mildew incidence was positively related to tree vigor. Our findings 37 reveal strong genetic, environmental, and G x E effects of disease on a foundation tree species, 38 and that particular environments can either enhance or diminish variation in responses among 39 tree genotypes. 40 41
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