Cytoskeletal Organization, its Evolution and Development, in Amphiesmenopteran Macrochaetae
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Cytoskeletal Organization, its Evolution and Development, in Amphiesmenopteran Macrochaetae

Abstract

This dissertation aims to bring new perspective to our understanding of the growth, development, and evolution of the vestiture which adorns the wings of the Lepidoptera—butterflies and moths. This perspective is wrought from both advancing imaging techniques to observe the growth of these elaborate cell-secreted structures directly and through examining parallel trends in the scales and bristles of their sister order, the Trichoptera—caddisflies. Firstly, I develop methods to observe at high resolution the organization, arrangement, and dynamics of the cytoskeleton and cellular organelles through early scale development using commercially available live cell dyes. These protocols permit observing any timepoint of wing growth for any butterfly and moth hindwing, and any wing surfaces of insect species with transparent pupal cuticle. These techniques help confirm that scales grow through actin filament elongation and subsequent bundling into thick rods and allow us to observe nuclear divisions and lineages of sensory organ precursors across species. Secondly, I correlate patterns of microtubule and actin filament distribution across scale types throughout the lepidopteran phylogeny and make an association between reticulated microtubule networks and flattened scale morphologies. I then identify a transcription factor that seems to specify a cylindrical, non-flattened, scale shape fate and tie this into the evolution of transparency and specialized, elongated androconial scales. Using live-imaging of microtubule networks across normal and drug-perturbed development, I connect these cytoskeletal and transcription factor data to hypothesize that this gene initiates a cellular program to stabilize microtubules, preventing their transition to a reticulate network and producing cylindrical cell shapes and that this fate switch has been used in the evolution of transparent wing patches and scent-dispersing scales throughout lepidopteran evolution. Lastly, I develop tools, including a genome, to study a genus of long-horned caddisflies, Nectopsyche, that has independently evolved scales resembling those of butterflies and moths, and present phylogenetic and morphological data to contextualize this convergence with our current knowledge of macrochaete cytoskeletal organization and the evolution of wing patterns. Altogether, this document establishes a first step in producing an understanding of comparative growth dynamics of amphiesmenopteran macrochaetae with an eye to uncover general trends linking cytoskeletal structure and cellular morphology.