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

Ting-Ru Mao, Ye-Wei Liu, View ORCID ProfileMadhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross, View ORCID ProfileMarcio R. Pie
doi: https://doi.org/10.1101/2020.04.12.038034
Ting-Ru Mao
1Guangxi Key Laboratory for Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi, P.R.C.
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Ye-Wei Liu
1Guangxi Key Laboratory for Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi, P.R.C.
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Madhava Meegaskumbura
1Guangxi Key Laboratory for Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi, P.R.C.
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Jian Yang
2Key Laboratory of Environment Change and Resource Use, Beibu Gulf, Nanning Normal University, Nanning, Guangxi, P.R.C.
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Gajaba Ellepola
1Guangxi Key Laboratory for Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi, P.R.C.
3Faculty of Science, University of Peradeniya, Peradeniya, KY 20400, Sri Lanka
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Gayani Senevirathne
4Department of Organismal Biology & Anatomy, University of Chicago, Chicago, IL, USA
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Cheng-Hai Fu
1Guangxi Key Laboratory for Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, Guangxi, P.R.C.
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Joshua B. Gross
5Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio, USA
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Marcio R. Pie
6Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil 81531-980
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  • ORCID record for Marcio R. Pie
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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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Errors in an institutional addresses corrected.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted April 14, 2020.
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Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Ting-Ru Mao, Ye-Wei Liu, Madhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross, Marcio R. Pie
bioRxiv 2020.04.12.038034; doi: https://doi.org/10.1101/2020.04.12.038034
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Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits
Ting-Ru Mao, Ye-Wei Liu, Madhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross, Marcio R. Pie
bioRxiv 2020.04.12.038034; doi: https://doi.org/10.1101/2020.04.12.038034

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