Influence of Genetic Variation in the Biotic Environment on Phenotypic Variation in a Plant-feeding Insect

Abstract

While many species spend much of their lives in close association with other organisms, only recently have biologists started to explore the implications of the biotic nature of environments for their role as causes of variation in phenotypes. This means that the genotypes of individuals that constitute the biotic environment may influence the phenotypes of individuals that live in that environment. These are called indirect genetic effects (IGEs) when they occur between conspecifics, and interspecific indirect genetic effects (IIGEs) when they occur between heterospecifics. However, the impact of genetic variation in biotic environments remains largely unknown. I used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess how male mating signals and female mate preferences are influenced by genetic variation in biotic environments. I used novel implementations of classic quantitative genetics designs, with samples of full-sibling families of treehoppers (IGEs) and clone lines of a sample of host plant genotypes (IIGEs) constituting the background biotic environment. To measure IGEs, I used full-sibling split-families as "treatment" social environments, and reared a random sample of focal females alongside each treatment family, describing the mate preferences of these focal females. With this I detected substantial genetic variation in social influence on mate preferences: the mate preferences of focal females varied according to the treatment families along with which they grew up. To measure IIGEs, I reared a random sample of treehoppers on potted replicates of a sample of host plant clones, describing the male signals and female mate preferences of these individuals. I found that male signals and female mate preferences varied according to the clone line on which they developed, demonstrating that genetic variation in host plants has cross-trophic consequences on sexually-selected traits at the level of the insect. I discuss the evolutionary implications of the presence of such genetic variation in biotic environments on male signals and female mate preferences. I focus on how IGEs and IIGEs may influence the way in which selection may act within and across environments, including potential contributions to the maintenance of genetic variation and the promotion of evolutionary divergence.