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Control Region Length Dynamics Potentially Drives Amino Acid Evolution in Tarsier Mitochondrial Genomes

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Abstract

Patterns and processes of molecular evolution critically influence inferences in phylogeny and phylogeography. Within primates, a shift in evolutionary rates has been identified as the rationale for contrasting findings from mitochondrial and nuclear DNA studies as to the position of Tarsius. While the latter now seems settled, we sequenced complete mitochondrial genomes of three Sulawesi tarsiers (Tarsius dentatus, T. lariang, and T. wallacei) and analyzed substitution rates among tarsiers and other primates to infer driving processes of molecular evolution. We found substantial length polymorphism of the D-loop within tarsier individuals, but little variation of predominant lengths among them, regardless of species. Length variation was due to repetitive elements in the CSB domain—minisatellite motifs of 35 bp length and microsatellite motifs of 6 bp length. Amino acid evolutionary rates were second highest among major primate taxa relative to nucleotide substitution rates. We observed many radical possibly function-altering amino acid changes that were rarely driven by positive selection and thus potentially slightly deleterious or neutral. We hypothesize that the observed pattern of an increased amino acid evolutionary rate in tarsier mitochondrial genomes may be caused by hitchhiking of slightly deleterious mutations with favored D-loop length variants selected for maximizing replication success within the cell or the mitochondrion.

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Acknowledgments

We thank the Indonesian authorities LIPI, RISTEK, PHKA, and BKSDA for granting research, capture, and export permits and the Primate Research Center at Bogor Agricultural University for providing administrative support. Nicolas Galtier and an anonymous reviewer provided valuable comments on an earlier draft of the manuscript. Sample collection, molecular analyses, and manuscript submission were supported through research grants from the Deutsche Forschungsgemeinschaft (DFG, Me2730/1-2, Me2730/1-3, and Me2730/2-1); the molecular work was partly supported by the research-funding program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Zoology, State Museum of Natural History Stuttgart, Rosenstein 1, 70191, Stuttgart, Germany

    Stefan Merker

  2. Evolutionary Ecology Group, Goethe University Frankfurt/M., Frankfurt/M., Germany

    Stefan Merker, Sarah Thomas, Elke Völker & Bruno Streit

  3. Primate Research Center, Bogor Agricultural University, Bogor, Indonesia

    Dyah Perwitasari-Farajallah

  4. Department of Evolutionary Biology, Johannes-Gutenberg University Mainz, Mainz, Germany

    Barbara Feldmeyer

  5. Molecular Ecology Group, Biodiversity and Climate Research Centre (BiK-F) by Senckenberg Gesellschaft für Naturforschung and Goethe-University, Frankfurt/M., Germany

    Markus Pfenninger

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  1. Stefan Merker
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  2. Sarah Thomas
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  3. Elke Völker
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Correspondence to Stefan Merker.

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Merker, S., Thomas, S., Völker, E. et al. Control Region Length Dynamics Potentially Drives Amino Acid Evolution in Tarsier Mitochondrial Genomes. J Mol Evol 79, 40–51 (2014). https://doi.org/10.1007/s00239-014-9631-2

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