Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes

Authors

  • K. R. ELMER,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • S. FAN,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • H. M. GUNTER,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • J. C. JONES,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • S. BOEKHOFF,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • S. KURAKU,

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • A. MEYER

    1. Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätstrasse 10, 78457 Konstanz, Germany
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  • The Meyer Laboratory (AM, KRE, JCJ, HGM, SF) is interested in the molecular basis of the vast ecological adaptations and evolutionary radiations of cichlid fishes, both African and neotropical. The Kuraku Laboratory (SK, SB) studies the evolution of gene repertoires, especially in early vertebrates, and the integration of bioinformatics and molecular evolutionary developmental biology.

Axel Meyer, Fax: +49 7531 88 3018;
E-mail: axel.meyer@uni-konstanz.de

Abstract

Crater lakes provide a natural laboratory to study speciation of cichlid fishes by ecological divergence. Up to now, there has been a dearth of transcriptomic and genomic information that would aid in understanding the molecular basis of the phenotypic differentiation between young species. We used next-generation sequencing (Roche 454 massively parallel pyrosequencing) to characterize the diversity of expressed sequence tags between ecologically divergent, endemic and sympatric species of cichlid fishes from crater lake Apoyo, Nicaragua: benthic Amphilophus astorquii and limnetic Amphilophus zaliosus. We obtained 24 174 A. astorquii and 21 382 A. zaliosus high-quality expressed sequence tag contigs, of which 13 106 pairs are orthologous between species. Based on the ratio of nonsynonymous to synonymous substitutions, we identified six sequences exhibiting signals of strong diversifying selection (Ka/Ks > 1). These included genes involved in biosynthesis, metabolic processes and development. This transcriptome sequence variation may be reflective of natural selection acting on the genomes of these young, sympatric sister species. Based on Ks ratios and p-distances between 3′-untranslated regions (UTRs) calibrated to previously published species divergence times, we estimated a neutral transcriptome-wide substitutional mutation rate of ∼1.25 × 10−6 per site per year. We conclude that next-generation sequencing technologies allow us to infer natural selection acting to diversify the genomes of young species, such as crater lake cichlids, with much greater scope than previously possible.

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