Genetic specificity of a plant–insect food web: Implications for linking genetic variation to network complexity

Abstract

Theory predicts that intraspecific genetic variation can increase the complexity of an ecological network. To date, however, we are lacking empirical knowledge of the extent to which genetic variation determines the assembly of ecological networks, as well as how the gain or loss of genetic variation will affect network structure. To address this knowledge gap, we used a common garden experiment to quantify the extent to which heritable trait variation in a host plant determines the assembly of its associated insect food web (network of trophic interactions). We then used a resampling procedure to simulate the additive effects of genetic variation on overall food-web complexity. We found that trait variation among host-plant genotypes was associated with resistance to insect herbivores, which indirectly affected interactions between herbivores and their insect parasitoids. Direct and indirect genetic effects resulted in distinct compositions of trophic interactions associated with each host-plant genotype. Moreover, our simulations suggest that food-web complexity would increase by 20% over the range of genetic variation in the experimental population of host plants. Taken together, our results indicate that intraspecific genetic variation can play a key role in structuring ecological networks, which may in turn affect network persistence.species interactions | ecological networks | evolutionary ecology | community genetics N etwork theory has provided both a conceptual and a quantitative approach for mapping interactions between species and making predictions about how the gain or loss of species will affect the structure and dynamics of ecological networks (1-3). Representing a network at the species level, however, makes the implicit assumption that each species consists of a homogenous population of individuals, all of which interact equally with individuals of different species. However, most populations are heterogeneous mixtures of individuals that vary in their phenotypes, and there is growing evidence that this intraspecific variation is an important factor governing the assembly of ecological communities (4-6). Consequently, there is a clear need to account for the role of intraspecific variation in structuring ecological networks (7).Genetic variation is a key driver of intraspecific variation and many studies have now demonstrated direct and indirect genetic effects on species interactions (8-10) and the composition of communities across multiple trophic levels (11)(12)(13)(14). This prior work forms a clear expectation that intraspecific genetic variation is capable of scaling up to affect the structure of an ecological network. In particular, we expect that network structure will be affected by genetic variation through at least two different mechanisms. For a food web (network of trophic interactions), genetic variation in the quality of a basal resource may alter the (i) abundances or (ii) phenotypes of consumer species or both (15). These direct genetic effects on consumers may then have cascadi...

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