Journal Article

Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits

Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R.

Record Number:
4788
Year:
2020
Journal:
bioRxiv preprint
Abstract:
Epitomized by the well-studied Astyanax mexicanus, cavefishes provide important model organisms to understand adaptations in response to divergent natural selection. However, the spectacular Sinocyclocheilus diversification of China, the most diverse cavefish clade in the world harboring nearly 75 species, demonstrate evolutionary convergence for many traits, yet remain poorly understood in terms of their morphological evolution. Here, using a broad sample of 49 species representative of this diversification, we analyze patterns of Sinocylocheilus evolution in a phylogenetic context. We categorized species into morphs based on eye-related condition: Blind, Micro-eyed (small-eyed), and Normal-eyed and we also considered three habitat types (Troglodytic – cave-restricted; Troglophilic – cave-associated; Surface – outside of caves). Geometric morphometric analyses show Normal-eyed morphs with fusiform shapes being segregated from Blind/Micro-eyed (Eye-regressed) morphs with deeper bodies along the first principal component (“PC”) axis. The second PC axis accounts for shape complexity related to the presence of horns. Ancestral character reconstructions of morphs suggest at least three independent origins of Blind morphs, each with different levels of modification in relation to the typical morphology of ancestral Normal-eyed morphs. Interestingly, only some Blind or Micro-eyed morphs bear horns and they are restricted to a single clade (Clade B) and arising from a Troglodytic ancestral species. Our geophylogeny shows an east-to-west diversification spanning the Pliocene and the Pleistocene, with Troglodytic species dominating karstic subterranean habitats of the plains whereas predominantly Surface species inhabit streams and pools in hills to the west (perhaps due to the scarcity of caves). Integration of morphology, phylogeny and geography suggests Sinocyclocheilus are pre-adapted for cave dwelling. Analyses of evolutionary rates suggest that lineages leading to Blind morphs were characterized by significant rate shifts, such as a slowdown in body size evolution and a 3.3 to 12.5 fold increase in the evolutionary rate of eye regression. Furthermore, body size and eye size have undergone reversals, but horns have not, a trait that seem to require substantial evolutionary time to form. These results, compared to the Astyanax model system, indicate Sinocyclocheilus fishes demonstrate extraordinary morphological diversity and variation, offering an invaluable model system to explore evolutionary novelty. KEYWORDS: Phylomorphospace, Evolutionary Convergence, Blind fish, Troglodytism, Geophylogeny, Pre-adaptation
Times Cited:
19
Related Records:
Yijing, Jie (1541)
[Report of a transparent fish in the Alu Limestone Cave, Yunnan, China. Possibly Sinocyclocheilus hyalinus]
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Morphometrics of eight Chinese cavefish species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
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A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Huang, Z., Titus, T., Postlethwait, J.H. and Meng, F. (2019)
Eye degeneration and loss of otx5b expression in the cavefish Sinocyclocheilus tileihornes
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Soares, D., Pluviose, M. and Zhao, Y. (2019)
Ontogenetic development of the horn and hump of the Chinese cavefish Sinocyclocheilus furcodorsalis (Cypriniformes: Cyprinidae)
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Policarpo, M., Fumey, J., Lafargeas, P., Legendre, L., Naquin, D., Thermes, C., Møller, P.R., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (2019)
Molecular decay of light-processing genes in cavefishes: assessing the effects of time, genome architecture and gene flow
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Policarpo, M., Fumey, J., Lafargeas, P., Legendre, L., Naquin, D., Thermes, C., Møller, P.R., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (2019)
Molecular decay of light-processing genes in cavefishes: assessing the effects of time, genome architecture and gene flow
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Luo, F., Huang, J., Shi, G., Luo, T., Liu, J. and Wen, Y. (2019)
Complete mitochondrial genome of Sinocyclocheilus yishanensis (Cypriniformes: Cyprinidae) and phylogenetic position.
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Chen, H., Li, C., Liu, T., Chen, S. and Xiao, H. (2019)
A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species
Lunghi, E., Zhao, Y., Sun, X. and Zhao, Y. (2019)
Morphometrics of eight Chinese cavefish species
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Policarpo, M., Fumey, J., Lafargeas, P., Naquin, D., Thermes, C., Naville, M., Dechaud, C., Volff, J.-M., Cabau, C., Klopp, C., Rask Møller, P., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (2020)
Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals
Policarpo, M., Fumey, J., Lafargeas, P., Naquin, D., Thermes, C., Naville, M., Dechaud, C., Volff, J.-M., Cabau, C., Klopp, C., Rask Møller, P., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (2020)
Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Mao, T.-R., Liu, Y.-W., Meegaskumbura, M., Yang, J., Ellepola, G., Senevirathne, G., Fu, C.-H., Gross, J.B. and Pie, M.R. (2020)
Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Policarpo, M., Fumey, J., Lafargeas, P., Naquin, D., Thermes, C., Naville, M., Dechaud, C., Volff, J.-M., Cabau, C., Klopp, C., Rask Møller, P., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (in press)
Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals
Policarpo, M., Fumey, J., Lafargeas, P., Naquin, D., Thermes, C., Naville, M., Dechaud, C., Volff, J.-M., Cabau, C., Klopp, C., Rask Møller, P., Bernatchez, L., García-Machado, E., Rétaux, S. and Casane, D. (in press)
Contrasted gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals