How Natural Pixel Arrays are Made: Unraveling the Genetics of Pattern Formation and Color Scale Specification in Butterfly Wings
Open Access DepositedBiological systems present immense robustness to environmental, genetic and stochastic variation, within which butterfly wings emerge as a prime model. Void of complexities during morphogenesis like tissue remodeling and cell migration, butterfly wings provide excellent study models to explore how morphogenetic processes provide links between genotypes and phenotypes. Adult wings are adorned by dense, orderly spaced and horizontally ordered scale cells that contain specific combinations of pigments and morphology. Morphogenetic processes begin in larval wing imaginal discs, in a similar way to the fly Drosophila, where the wing tissue is specified in terms of dorsal-ventral and anterior-posterior axes. Of note, unlike in Drosophila, butterfly wing imaginal discs do not evert, such that both proximodistal and anterior-posterior axes of the imaginal discs resemble the final adult wing, with the additional basal matrix separating the apposing ventral and dorsal surfaces. Upon metamorphosis, wing morphogenesis involves the structural remodeling of veins and margin, during which specification of sensory organ precursors (SOPs) results in two successive rounds of division to produce scale- and socket-building cells, processes largely similar to those to produce bristle-producing cells on Drosophila wings. Thanks to the robust development of wings, our current understanding of pupal wing morphogenesis has been furthered by the flexibility to manipulate the system for in vivo live imaging, where lineage reconstruction can recover the timing of division, scale formation and structural elaboration. Dissecting the development of butterfly wing color patterns is key to understanding the basic principles guiding the bauplan of this two dimensional, bilayered epithelial tissue. While the past century of work in lepidoptera revealed a fundamental ground plan upon which deviations produce diverse wing color patterns, a chronological profile of molecular factors from gene regulatory networks at different timepoints remains unknown. This work serves to identify key genetic players of three main processes of butterfly wing development in the pupa, 1) the prepatterning of pattern compartment boundaries, 2) the determination of scale cell identities 3) the generation of elaborate extracellular cuticular processes. By comparing with the established Drosophila model, lepidopteran scale development provides additional mechanistic insights into how to remodel a canonical differentiation program to produce scales built from the same cellular architecture, but different in their optical properties. The 1-to-1 genotype to phenotype correlation of scale-building cell to the ‘pixel’ on the wing presents lepidopteran wing scales as a powerful system to address developmental questions. These questions range from how pattern boundaries are specified in Chapter 2, how cell fates are acquired during rapid mitotic divisions and endocycling events that drive cellular and tissue growth in Chapter 3, to cell-autonomous acquisition of sexual identity that confers a distinct secondary sexual trait in Chapter 4. Ultimately, this work uses butterfly wing scale development to shed light on how diverse phenotypes arise by manipulating processes during development.
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