Homeostatic and circadian mechanisms of bioluminescence regulation differ between a forest and a facultative cave species of glowworm, Arachnocampa

Abstract

Glowworms, members of the keroplatid fly genus, Arachnocampa, glow to attract prey. Here we describe substantial differences in the bioluminescence regulatory systems of two species; one is a troglophile with populations both in caves and outside of caves in wet forest (Arachnocampa tasmaniensis) and the other has no known cave populations (Arachnocampa flava). We find that A. tasmaniensis is ready to initiate bioluminescence at any time darkness is encountered. In contrast, A. flava shows a homeostatic control of bioluminescence; it is unlikely to initiate bioluminescence when exposed to dark pulses during the photophase and it does so with a long latency. Another difference between the two species is that A. tasmaniensis individuals synchronize their bioluminescence in the dark zone of caves under the control of the circadian system and A. flava individuals do not synchronize to each other, rather their circadian control system entrains to the light:dark cycle to promote nocturnal bioluminescence. Consequently, we produced a phase-response curve in response to photic entrainment under constant darkness for both species. The shape of the phase-response curves differs between the two species as does the overall sensitivity to the identical entrainment conditions. The phase-response curve of A. tasmaniensis facilitates synchronization whereas that of A. flava facilitates nocturnal glowing. The two-species comparison highlights possible pathways of divergence of circadian control of physiological functions that could be associated with the extreme ecological differences experienced in cave and surface habitats.