Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum

Background: Two visual systems are present in most arthropod groups: median and lateral eyes. Most of our current knowledge about the developmental and molecular mechanisms involved in eye formation in arthropods comes from research in the model system Drosophila melanogaster. Here, a core set of retinal determination genes, namely, sine-oculis (so), eyes absent (eya), dachshund (dac), and the two pax6 orthologues eyeless (ey) and twin of eyeless (toy) govern early retinal development. By contrast, not much is known about the development of the up-to-eight eyes present in spiders. Therefore, we analyzed the embryonic expression of core retinal determination genes in the common house spider Parasteatoda tepidariorum. Results: We show that the anlagen of the median and lateral eyes in P. tepidariorum originate from different regions of the non-neurogenic ectoderm in the embryonic head. The median eyes are specified as two individual anlagen in an anterior median position in the developing head and subsequently move to their final position following extensive morphogenetic movements of the non-neurogenic ectoderm. The lateral eyes develop from a more lateral position. Intriguingly, they are specified as a unique field of cells that splits into the three individual lateral eyes during late embryonic development. Using gene expression analyses, we identified a unique combination of determination gene expression in the anlagen of the lateral and median eyes, respectively. Conclusions: This study of retinal determination genes in the common house spider P. tepidariorum represents the first comprehensive analysis of the well-known retinal determination genes in arthropods outside insects. The development of the individual lateral eyes via the subdivision of one single eye primordium might be the vestige of a larger composite eye anlage, and thus supports the notion that the composite eye is the plesiomorphic state of the lateral eyes in arthropods. The molecular distinction of the two visual systems is similar to the one described for compound eyes and ocelli in Drosophila, suggesting that a unique core determination network for median and lateral eyes, respectively, might have been in place already in the last common ancestor of spiders and insects.