Eyeless cave-dwelling Leptonetela spiders still rely on light

Abstract

Subterranean animals living in perpetual darkness may maintain photoresponse. However, the evolutionary processes behind the conflict between eye loss and maintenance of the photoresponse remain largely unknown. We used Leptonetela spiders to investigate the driving forces behind the maintenance of the photoresponse in cave-dwelling spiders. Our behavioral experiments showed that all eyeless/reduced-eyed cave-dwelling species retained photophobic response and that they had substantially decreased survival at cave entrances due to weak drought resistance. The transcriptomic analysis demonstrated that nearly all phototransduction pathway genes were present and that all tested phototransduction pathway genes were subjected to strong functional constraints in cave-dwelling species. Our results suggest that cave-dwelling eyeless spiders still use light and that light detection likely plays a role in avoiding the cave entrance habitat. This study confirms that some eyeless subterranean animals have retained their photosensitivity due to natural selection and provides a case of mismatch between phenotype and genotype or physiological function in a long-term evolutionary process.