Bolwig Organ and Its Role in the Photoperiodic Response of Sarcophaga similis Larvae

SIMPLE SUMMARY: The flesh fly Sarcophaga similis shows a clear photoperiodic response, in which its larvae enter pupal diapause as a response to short days, for seasonal adaptation. Although sensitive wavelengths for photoperiodic photoreception have been demonstrated, the photoreceptor organ remains unclear. The aim of this study was to identify the Bolwig organ, a known fly larval-photoreceptor, in S. similis and to determine whether the Bolwig organ is the photoperiodic photoreceptor. The Bolwig organ, consisting of more than 30 cells, was located as a tiny spherical body attached to the internal skeleton in the anterior region of S. similis larvae. Bolwig-organ neurons extend fibres to terminate near putative circadian-clock neurons in the brain. Surgical ablation of the Bolwig organ cancelled photoperiodic responses, and the incidence of diapause after the surgery was similar to that of intact larvae reared under constant darkness. This suggests that the Bolwig organ partially contributes to photoperiodic photoreception, and other photoreceptors may also be involved. This finding opens the door for the investigation of the neural mechanisms of insect photoperiodism using the simple larval brain of S. similis. ABSTRACT: Flesh-fly Sarcophaga similis larvae exhibit a photoperiodic response, in which short days induce pupal diapause for seasonal adaptation. Although the spectral sensitivity of photoperiodic photoreception is known, the photoreceptor organ remains unclear. We morphologically identified the Bolwig organ, a larval-photoreceptor identified in several other fly species, and examined the effects of its removal on the photoperiodic response in S. similis. Backfill-staining and embryonic-lethal-abnormal-vision (ELAV) immunohistochemical-staining identified ~34 and 38 cells, respectively, in a spherical body at the ocular depression of the cephalopharyngeal skeleton, suggesting that the spherical body is the Bolwig organ in S. similis. Forward-fill and immunohistochemistry revealed that Bolwig-organ neurons terminate in the vicinity of the dendritic fibres of pigment-dispersing factor-immunoreactive and potential circadian-clock neurons in the brain. After surgical removal of the Bolwig-organ regions, diapause incidence was not significantly different between short and long days, and was similar to that in the insects with an intact organ, under constant darkness. However, diapause incidence was not significantly different between the control and Bolwig-organ-removed insects for each photoperiod. These results suggest that the Bolwig organ contributes partially to photoperiodic photoreception, and that other photoreceptors may also be involved.