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bioRxiv · 10.1101/2023.08.31.555641

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

Chen, B.·Dai, W.-Z.·Li, X.-L.·Mao, T.-R.·Liu, Y.·Pie, M. R.·Yang, J.·Meegaskumbura, M.
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Abstract

With 75 known species, the freshwater-fish genus Sinocyclocheilus is the largest cavefish radiation in the world, emerging as a model system for evolutionary studies. They show multiple adaptations for cave dwelling (stygomorphic adaptations), which include a range of traits such as eye degeneration (Normal-eyed, Micro-eyed and Eyeless), depigmentation of skin, and in some species, the presence of "horns". Their behavioural adaptations to subterranean environments, however, are poorly understood. Wall-following (WF) behaviour, where an organism remains in close contact with the boundary demarcating its habitat when in the dark, is a peculiar behaviour observed in a wide range of animals and is enhanced in some cave dwellers. Hence, we hypothesize wall-following to be present also in Sinocyclocheilus, possibly enhanced in Eyeless species compared to species with visual cues (Normal / Micro-eyed species). Using 13 species representative of Sinocyclocheilus radiation and eye-morphs, we designed a series of assays, based on pre-existing methods for Astyanax mexicanus behavioural experiments, to examine wall-following behaviour under three stimulation conditions. Our results indicate that eyeless species exhibit significantly enhanced levels of WF compared to Normal-eyed species, with Micro-eyed forms demonstrating intermediate levels. Using a mtDNA based dated phylogeny (chronogram with four clades A - D), we traced the degree of WF of these forms to outline common patterns. We show that intensity of WF behaviour is high in the subterranean clades (B & C) compared to clades with free-living species (A & D). Experiments on WF behaviour revealed that eyeless species are highly sensitive to vibrations, whereas normal-eyed species are the least sensitive. Since WF behaviour is present to some degree in all Sinocyclocheilus species, and given that these fishes evolved in the late Miocene, we identify this behaviour as being ancestral with WF enhancement related to cave occupation. Our results from this diversification-scale study of cavefish behaviour suggest that enhanced wall-following behaviour may be a convergent trait across all stygomorphic cavefish lineages. Significance statementSinocyclocheilus, a genus of 75 species of freshwater cavefish, is an emerging model system in evolutionary studies. Their adaptations for subterranean life, including eye degeneration, skin depigmentation, and horn-like structures, are well-known, but their behavioural adaptations remain understudied. Here we focus on a phenomenon, called "wall-following," where fish stay close to the cave walls in absence of light. We hypothesized that this behaviour would be more pronounced in eyeless species. We selected 13 species, representative of the diversity of the genus and eye types, and observed their wall-following behaviour under different conditions. Results were intriguing; eyeless species exhibited heightened wall-following behaviour compared to their sighted counterparts, with small-eyed species falling in between. Researchers also mapped this behaviour on a phylogenetic tree, discovering a pattern: cave-dwelling clades showed stronger wall-following than free-living ones. Wall-following is prevalent in all Sinocyclocheilus species and, given the evolutionary history of the genus, is considered an ancestral behaviour that intensified with cave adaptation. These findings contribute to our understanding of convergent evolution, suggesting that enhanced wall-following may be a shared trait among diverse cavefish lineages.

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Chen, B., Dai, W.-Z., Li, X.-L., Mao, T.-R., Liu, Y., Pie, M. R., Yang, J., Meegaskumbura, M.. 2023-09-01. Wall-following: phylogenetic context of an enhanced behaviour in stygomorphic Sinocyclocheilus (Cypriniformes: Cyprinidae) cavefishes. https://doi.org/10.1101/2023.08.31.555641

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