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Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua

Authors

  • Tereza Manousaki,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    2. Konstanz Research School Chemical Biology (KoRS-CB), University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
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    • Co-first authors.
  • Pincelli M. Hull,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    2. Department of Geology and Geophysics, Yale University, New Haven, CT, USA
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    • Co-first authors.
  • Henrik Kusche,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    2. International Max Planck Research School for Organismal Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
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  • Gonzalo Machado-Schiaffino,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
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  • Paolo Franchini,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
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  • Chris Harrod,

    1. Department of Evolutionary Genetics, Max Planck Institute for Limnology, Plön, Germany
    2. School of Biological Sciences, Queen's University, Belfast, UK
    3. Instituto de Investigaciones Oceanológicas, Universidad de Antofagasta, Antofagasta, Chile
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  • Kathryn R. Elmer,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    Current affiliation:
    1. College of Medical, Veterinary & Life Sciences, Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow, UK
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  • Axel Meyer

    Corresponding author
    1. Konstanz Research School Chemical Biology (KoRS-CB), University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    2. International Max Planck Research School for Organismal Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
    • Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstrasse 10, Konstanz, Germany
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Correspondence: Axel Meyer, Fax: +49 7531 883018; E-mail: axel.meyer@uni-konstanz.de

Abstract

The study of parallel evolution facilitates the discovery of common rules of diversification. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex)—from two Great Lakes and two crater lakes in Nicaragua—to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expression in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underexpressed in the thick-lipped morph across all four lakes. However, other aspects of lips' gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (δ13C and δ15N) differ between all sympatric morphs, with the greatest differentiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution.

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