Testing how an ancient eye development plan gives rise to camera-type eyes

Vertebrates, including humans, have relatively similar eyes, but invertebrates exhibit an extraordinary diversity of visual systems, with a wide range of designs, from compound eyes to systems composed of multiple image-forming units that work together. These visual systems are highly specialized, each comprising a unique way to process visual information and often optimized for specific tasks. Understanding how such complex and varied eyes develop can provide new insights into both biology and technology. Indeed, previous research by the principal investigator has inspired the design of innovative camera systems based on the organization of insect eyes. The current project goes a step further by leveraging a computational model (EyeVolve) developed in the host laboratory that explains how different eye structures may arise during development through the arrangement of specialized cell types. This project will test that model by studying the development of visual systems in two insect species that are thought to represent two major evolutionary pathways between distinct modes of vision. By comparing these species and testing specific predictions of the model, the project aims to uncover the developmental mechanisms that generate diverse optical systems. Improved understanding of how evolution has shaped fundamental developmental processes will advance knowledge of how visual systems evolve and function and may guide the development of new biotechnologies inspired by nature. In particular, uncovering the principles by which living organisms build specialized visual systems could inform the design of next-generation imaging devices, autonomous sensors, and adaptive optical technologies that perform efficiently in complex environments. The project will provide research and training opportunities for undergraduate and graduate students and will include the development of public-facing educational and outreach activities. Several arthropods have high-resolution camera-type eyes with hundreds of photoreceptors. Functionally, these are more similar to our own than to compound eyes, but almost nothing is known about how development gives rise to these organizations. The EyeVolve model illustrates how two different developmental mechanisms (expansion and fusion) could result in camera-type eyes, identifying specific genes likely involved, as well as correlated patterns of photoreceptor placement. Previous work by the host laboratory on sunburst diving beetle larvae Thermonectus marmoratus, highly specialized visually guided predators, suggests that their sophisticated camera eyes evolved through expansion. Related hypotheses will be assessed by testing a variety of specific predictions regarding related developmental processes. Hybridization Chain Reaction in situ staining, RNAi-based knockdown, and comparative transcriptomics will be used to evaluate the roles of specific genes in this process. The other developmental mode, which involves the initial formation of many ommatidial units that subsequently fuse into a single camera-type eye, is a likely scenario for the single stemma on each side of the head of the sawfly Neodiprion lecontei. Here, specific predictions will be tested pertaining to later developmental processes involving support cells, for which our preliminary data suggest that the transcription factor cut and atonal play a major role. It is expected that this integrative approach will provide important fundamental insights into how biological image-processing systems develop. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.