Transcriptomic insights into the loss of vision in Molnár János Cave’s crustaceans

Abstract

Animals that inhabit subterranean environments often undergo various distinct phenotypic modifications (referred to as "troglomorphy") as they transition to life in perpetual darkness. However, the molecular basis behind troglomorphy remains poorly understood, particularly in regards to the mechanisms involved in the reduction and/or loss of traits at the transcriptomic level. In this study we investigate the transcriptional basis behind vision loss in populations of cave-dwelling crustaceans. We employ phylogenetic and transcriptomic methods on surface and cave-adapted populations of an emerging model species for biospeleology, the isopod Asellus aquaticus (Linnaeus, 1758), and the amphipod Niphargus hrabei S. Karaman, 1932. These two species show contrasting directionality in the surface-cave transition, which positions them as ideal study subjects. A. aquaticus is common in surface waters and is only occasionally found in caves, where its populations present different degrees of eye reduction and pigmentation. On the other hand, the eyeless N. hrabei has successfully colonized surface environments despite belonging to an almost exclusively cave-dwelling genus. By sequencing and assembling robust de novo transcriptomes we characterized differences in visual genes and pathways among surface and cave populations of the aforementioned species. Our results indicate that despite having reduced eyes, recent cave colonizer A. aquaticus is still capable of expressing functional visual opsins and major components of the phototransduction pathway within the cave. Niphargus hrabei, a species with an ancient cave origin, shows no clear indication of being capable of sight. However, the expression of putative functional visual opsins and other phototransduction genes was maintained, which suggests that this eyeless species might be capable of extraocular photoreception. With the present study, we aim to bring forth the Molnár János Cave system as a promising research avenue to improve our understanding of patterns of reduction and loss of vision in caves and other aphotic environments.