Vision is among the oldest and arguably most important sensory modalities for animals to interact with their external environment. Although many different eye types exist within the animal kingdom, mounting evidence indicates that the genetic networks required for visual system formation and function are relatively well conserved between species. This raises the question as to how common developmental programs are modified in functionally different eye types. Here, we approached this issue through EyeVolve, an open-source PYTHON-based model that recapitulates eye development based on developmental principles originally identified in Drosophila melanogaster . Proof-of-principle experiments showed that this program’s animated timeline successfully simulates early eye tissue expansion, neurogenesis, and pigment cell formation, sequentially transitioning from a disorganized pool of progenitor cells to a highly organized lattice of photoreceptor clusters wrapped with support cells. Further, tweaking just five parameters (precursor pool size, founder cell distance and placement from edge, photoreceptor subtype number, and cell death decisions) predicted a multitude of visual system layouts, reminiscent of the varied eye types found in larval and adult arthropods. This suggests that there are universal underlying mechanisms that can explain much of the existing arthropod eye diversity. Thus, EyeVolve sheds light on common principles of eye development and provides a new computational system for generating specific testable predictions about how development gives rise to diverse visual systems from a commonly specified neuroepithelial ground plan.
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A mosaic of independent innovations involving eyes shut are critical for the evolutionary transition from fused to open rhabdoms
A fundamental question in evolutionary biology is how developmental processes are modified to produce morphological innovations while abiding by functional constraints. Here we address this question by investigating the cellular mechanism responsible for the transition between fused and open rhabdoms in ommatidia of apposition compound eyes; a critical step required for the development of visual systems based on neural superposition. Utilizing Drosophila and Tribolium as representatives of fused and open rhabdom morphology in holometabolous insects respectively, we identified three changes required for this innovation to occur. First, the expression pattern of the extracellular matrix protein Eyes Shut (EYS) was co-opted and expanded from mechanosensory neurons to photoreceptor cells in taxa with open rhabdoms. Second, EYS homologs obtained a novel extension of the amino terminus leading to the internalization of a cleaved signal sequence. This amino terminus extension does not interfere with cleavage or function in mechanosensory neurons, but it does permit specific targeting of the EYS protein to the apical photoreceptor membrane. Finally, a specific interaction evolved between EYS and a subset of Prominin homologs that is required for the development of open, but not fused, rhabdoms. Together, our findings portray a case study wherein the evolution of a set of molecular novelties has precipitated the origin of an adaptive photoreceptor cell arrangement.
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- Award ID(s):
- 1353267
- NSF-PAR ID:
- 10077424
- Date Published:
- Journal Name:
- Developmental biology
- ISSN:
- 0012-1606
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Basic Protocol 1 : Lentivirus production and expression line creationSupport Protocol 1 : Six‐well assay for estimation of production cell line yieldSupport Protocol 2 : Universal ELISA for quantifying proteins with fused leucine zippers and His‐tagsBasic Protocol 2 : Cultures for production of Class II MHC proteinsBasic Protocol 3 : Purification of Class II MHC proteins by anti‐leucine zipper affinity chromatographyAlternate Protocol 1 : IMAC purification of His‐tagged Class II MHCSupport Protocol 3 : Protein concentration measurements and adjustmentsSupport Protocol 4 : Polishing purification by anion‐exchange chromatographySupport Protocol 5 : Estimating biotinylation percentage by streptavidin precipitationBasic Protocol 4 : Peptide exchangeBasic Protocol 5 : Analysis of peptide exchange by matrix‐assisted laser desorption/ionization (MALDI) mass spectrometryAlternate Protocol 2 : Native isoelectric focusing to validate MHC‐II peptide loadingBasic Protocol 6 : MultimerizationBasic Protocol 7 : Staining cells with Class II MHC tetramers
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