Cave habitats are remarkable environments for the study of biological adaptations and morphological convergence. One compelling trait that has repeatedly evolved in cave-dwelling organisms is loss of the eyes. Predatory arthropods like arachnids (e.g., spiders and harvestmen) play an important role in cave ecosystems and the group includes many examples of cave-adapted blind species. However, remarkably little is known about how arachnid eyes develop, much less how these eyes are lost in cave-specialized arachnids. This binational project brings together a US-Israeli team to advance understanding the evolutionary developmental biology of arachnid eyes. To examine how eyes are lost in cave-adapted arachnids, embryonic development will be compared for a sister-species pair in each of three arachnid orders (spiders, whip spiders, and harvestmen) that will be collected through intensive fieldwork campaigns; in each pair, a surface species bears eyes and its sister species is blind. To determine the genomic basis for eye degeneration, high-quality reference genomes will be established for these six species, together with profiling of gene expression using parallelized short read sequencing. To validate predictions of key genes putatively underlying cave adaptations that are inferred from genomic datasets, gene silencing screens will be performed in two model arachnid species, with the goal of establishing a direct link between patterns observed in nature and functional datasets in the laboratory.
By comparison to better-studied vertebrate and pancrustacean (e.g., insects; isopod crustaceans) models, eye development in Chelicerata remains poorly studied. With respect to the developmental genetics of arachnid eyes, no datasets are available beyond in situ hybridization assays; even the morphogenesis of arachnid eyes remains underexplored from the perspective of modern imaging toolkits, relative to vertebrate and pancrustacean counterparts. Yet, the arachnid eye is of interest from the standpoint of comparative biology for two reasons. First, in contrast to the main pair of compound (faceted) eyes of pancrustaceans, arachnids bear multiple eye pairs broadly divided into two types of ocelli, which are structurally and functionally distinct from each other. A further complexity of arachnids is that a subset of orders that includes lineages like scorpions and spiders has undergone a shared genome duplication, resulting in numerous paralogs of retinal determinal gene network (RDGN) homologs, which are involved in patterning eyes of many other bilaterian groups. The proposed work will interrogate the development of arachnid eyes using a comparative framework that samples three key arachnid orders, toward establishing a comparative platform incorporating independently evolving lineages for study of cave biology, as well as for understanding the evolution of paralog function after genome duplication. Beyond establishing new model systems for study of arthropod development, this research will establish new genomic resources and toolkits for deciphering the evolution of developmental processes inferred from naturally evolving cave systems.
This research award from the Directorate of Biological Sciences is funded by the Developmental Systems and EDGE Programs within the Division of Integrative and Organismal Systems, and by the Evolutionary Processes Program within the Division of Environmental Biology.
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.
