Ontogenetic trajectories and early shape differentiation of treehopper pronota (Hemiptera: Membracidae).

Membracids (family: Membracidae), commonly known as treehoppers, are recognizable by their enlarged and often elaborated pronota. Much of the research investigating the development and evolution of this structure has focused on the fifth instar to adult transition, in which the pronotum undergoes the largest transformation as it takes on adult identity. However, little is known about the earlier nymphal stages, the degree to which the pronotum develops at these timepoints, and how development has changed relative to the ancestral state. Here, we studied the nymphal stages and adults of five morphologically distinct membracid species and of Aetalion reticulatum (family: Aetalionidae), the outgroup which was used as an ancestral state proxy. We found that shape differentiation in the pronotum of membracids can start as early as the second instar stage. Most shape differentiation occurs within the nymphal stages and not in the embryo since the shape of the first-instar pronotum did not differ from the outgroup species in all but one species we investigated. We found the anterior-posterior axis of the pronotum elongated at a faster relative rate in membracid species than in A. reticulatum, which contributed to the development of exaggerated pronotal size. Finally, we found differences in the morphogenesis of shape across species. We suggest this is due to the developmental and evolutionary divergence of differential growth patterning of the dorsal surface of the pronotum, not only across species, but also between stages within the same species. This lability may contribute to the evolvability and diversification of the membracid pronotum.

The roles of growth regulation and appendage patterning genes in the morphogenesis of treehopper pronota.

Treehoppers of the insect family Membracidae have evolved enlarged and elaborate pronotal structures, which is hypothesized to involve co-opted expression of genes that are shared with the wings. Here, we investigate the similarity between the pronotum and wings in relation to growth. Our study reveals that the ontogenetic allometry of the pronotum is similar to that of wings in Membracidae, but not the outgroup. Using transcriptomics, we identify genes related to translation and protein synthesis, which are mutually upregulated. These genes are implicated in the eIF2, eIF4/p70S6K and mTOR pathways, and have known roles in regulating cell growth and proliferation. We find that species-specific differential growth patterning of the pronotum begins as early as the third instar, which suggests that expression of appendage patterning genes occurs long before the metamorphic molt. We propose that a network related to growth and size determination is the more likely mechanism shared with wings. However, regulators upstream of the shared genes in pronotum and wings need to be elucidated to substantiate whether co-option has occurred. Finally, we believe it will be helpful to distinguish the mechanisms leading to pronotal size from those regulating pronotal shape as we make sense of this spectacular evolutionary innovation.

Genetic assimilation and accommodation: Models and mechanisms.

Genetic assimilation and genetic accommodation are mechanisms by which novel phenotypes are produced and become established in a population. Novel characters may be fixed and canalized so they are insensitive to environmental variation, or can be plastic and adaptively responsive to environmental variation. In this review we explore the various theories that have been proposed to explain the developmental origin and evolution of novel phenotypes and the mechanisms by which canalization and phenotypic plasticity evolve. These theories and models range from conceptual to mathematical and have taken different views of how genes and environment contribute to the development and evolution of the properties of phenotypes. We will argue that a deeper and more nuanced understanding of genetic accommodation requires a recognition that phenotypes are not static entities but are dynamic system properties with no fixed deterministic relationship between genotype and phenotype. We suggest a mechanistic systems-view of development that allows one to incorporate both genes and environment in a common model, and that enables both quantitative analysis and visualization of the evolution of canalization and phenotypic plasticity.