Sensory evolution in a cavefish radiation: patterns of neuromast distribution and associated behaviour inSinocyclocheilus(Cypriniformes: Cyprinidae)

Abstract

The genus Sinocyclocheilus , comprising a large radiation of freshwater cavefishes, are well known for their presence of regressive features (e.g. variable eye reduction). Fewer constructive features are known, such as the expansion of the lateral line system (LLS), which is involved in detecting water movements. The precise relationship between LLS expansion and cave adaptation is not well understood. Here, we examine morphology and LLS-mediated behaviour in Sinocyclocheilus species characterized by broad variation in eye size, habitat and geographical distribution. Using live-staining techniques and automated behavioural analyses, we examined 26 Sinocyclocheilus species and quantified neuromast organ number, density and asymmetry within a phylogenetic context. We then examined how these morphological features may relate to wall-following, an established cave-associated behaviour mediated by the lateral line. We show that most species demonstrated laterality (i.e. asymmetry) in neuromast organs on the head, often biased to the right. We also found that wall-following behaviour was distinctive, particularly among eyeless species. Patterns of variation in LLS appear to correlate with the degree of eye loss, as well as geographical distribution. This work reveals that constructive LLS evolution is convergent across distant cavefish taxa and may mediate asymmetric behavioural features that enable survival in stark subterranean microenvironments.

Wall-following – phylogenetic context of an enhanced behaviour in stygomorphicSinocyclocheilus(Cypriniformes: Cyprinidae) cavefishes

“…This spatial exploratory behaviour also associated with the enhanced olfactory system and lateral line systems in cavefishes (Fernandes et al, 2018;Kasumyan and Marusov, 2018;Lloyd et al, 2018;Chen et al, 2022b).…”

“…This could indicate an ability to detect unknown objects at longer distances in Normal-eyed species, reflecting differences in sensory capabilities and risk assessment strategies among the species. This spatial exploratory behaviour also associated with the enhanced olfactory system and lateral line systems in cavefishes (Fernandes et al, 2018; Kasumyan and Marusov, 2018; Lloyd et al, 2018; Chen et al, 2022b).…”

“…To occupy caves, species became adapted to the low availability of resources such as light, oxygen concentration and nutrients, leading to stygomorphic adaptations, including elongated appendages, lowered metabolism, specialized sensory systems, loss of eyes and pigmentation (Yoshizawa et al, 2012; Jeffery, 2019; Chen et al, 2020; Li et al, 2020; Ma et al, 2020a). A prominent stygomorphic convergent feature of cavefishes is the degeneration of eyes, compensated for by enhancements to the mechanosensory organs such as the neuromast lateral line system (Borowsky, 2013; Ma et al, 2020b; Chen et al, 2022b). A prominent swimming behaviour of cavefish is wall-following (WF, a form of thigmotaxis), where the fish senses the walls or boundaries of its cave environment in the absence of visual cues (Sharma et al, 2009; Patton et al, 2010).…”

“…For instance, S. grahami (Normal-eyed, Surface-dwelling) swim faster and farther, swimming at a speed 2-3 times greater than S. anshuiensis (Zheng, 2017). The neuromast system in Sinocyclocheilus has been shown to be asymmetric and is correlated with the degree of eye-degeneration and is pronounced in the eyeless forms (Chen et al 2022b). Furthermore, for several species, the wall-following behaviour is also thought to be associated with neuromast asymmetry, with eyeless forms having the strongest WF behaviours (Chen at al.…”

“…For instance, S. grahami (Normal-eyed, Surface-dwelling) swim faster and farther, swimming at a speed 2-3 times greater than S. anshuiensis (Zheng, 2017). The neuromast system in Sinocyclocheilus has been shown to be asymmetric and is correlated with the degree of eye-degeneration and is pronounced in the eyeless forms (Chen et al 2022b).…”