Characterization of eyes, photoreceptors, and opsins in developmental stages of the arrow wormSpadella cephaloptera(Chaetognatha)

Abstract

AbstractThe phylogenetic position of chaetognaths, or arrow worms, has been debated for decades, however recently they have been grouped into the Gnathifera, a sister clade to all other Spiralia. Chaetognath photoreceptor cells are anatomically unique by exhibiting a highly modified cilium and are arranged differently in the eyes of the various species. Studies investigating eye development and underlying gene regulatory networks are so far missing. To gain insights into the development and the molecular toolkit of chaetognath photoreceptors and eyes a new transcriptome of the epibenthic speciesSpadella cephalopterawas searched for opsins. Our screen revealed two copies ofxenopsinand a single copy ofperopsin. Gene expression analyses demonstrated that onlyxenopsin1is expressed in photoreceptor cells of the developing lateral eyes. Adults likewise exhibit twoxenopsin1 + photoreceptor cells in each of their lateral eyes. Beyond that, a singlecryptochromegene was uncovered and found to be expressed in photoreceptor cells of the lateral developing eye. In addition,cryptochromeis also expressed in the cerebral ganglia in a region in which alsoperopsinexpression was observed. This condition is reminiscent of a nonvisual photoreceptive zone in the apical nervous system of the annelidPlatynereis dumeriliithat performs circadian entrainment and melatonin release.Cryptochromeis also expressed in cells of the corona ciliata, an organ in the posterior dorsal head region, indicating a role in circadian entrainment. Our study highlights the importance of the Gnathifera for unraveling the evolution of photoreceptors and eyes in Spiralia and Bilateria.