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Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey

Nature Genetics volume 30, pages 411–415 (2002)Cite this article

Abstract

Although the complete genome sequences of over 50 representative species have revealed the many duplicated genes in all three domains of life1,2,3,4, the roles of gene duplication in organismal adaptation and biodiversity are poorly understood. In addition, the evolutionary forces behind the functional divergence of duplicated genes are often unknown, leading to disagreement on the relative importance of positive Darwinian selection versus relaxation of functional constraints in this process5,6,7,8,9,10. The methodology of earlier studies relied largely on DNA sequence analysis but lacked functional assays of duplicated genes, frequently generating contentious results11,12. Here we use both computational and experimental approaches to address these questions in a study of the pancreatic ribonuclease gene (RNASE1) and its duplicate gene (RNASE1B) in a leaf-eating colobine monkey, douc langur. We show that RNASE1B has evolved rapidly under positive selection for enhanced ribonucleolytic activity in an altered microenvironment, a response to increased demands for the enzyme for digesting bacterial RNA. At the same time, the ability to degrade double-stranded RNA, a non-digestive activity characteristic of primate RNASE1, has been lost in RNASE1B, indicating functional specialization and relaxation of purifying selection. Our findings demonstrate the contribution of gene duplication to organismal adaptation and show the power of combining sequence analysis and functional assays in delineating the molecular basis of adaptive evolution.

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Figure 1: Protein sequences and genomic structures of RNASE1 and RNASE1B of primates.
Figure 2: Phylogenetic relationships among RNASE1 and RNASE1B of primates.
Figure 3: Tests of the molecular clock hypothesis for RNASE1 and RNASE1B of douc langur.
Figure 4: Enzyme activities of recombinant RNASE1B, RNASE1 and mutant forms of RNASE1.

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Acknowledgements

We thank K. Dyer for technical assistance and J. Beintema, A. Rooney and three anonymous referees for their comments on early versions of the manuscript. This work was supported in part by a start-up fund and a Rackham grant from the University of Michigan (to J.Z.) and grants from the Natural Science Foundation of China and Chinese Academy of Sciences (to Y.P.Z.).

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Authors and Affiliations

  1. Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA

    Jianzhi Zhang & Helene F. Rosenberg

  2. Departments of Ecology and Evolutionary Biology and Molecular, Cellular and Developmental Biology, University of Michigan, 3003 Natural Sciences Building, 830 North University Avenue, Ann Arbor, 48109, Michigan, USA

    Jianzhi Zhang

  3. Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China

    Ya-ping Zhang

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  1. Jianzhi Zhang
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Correspondence to Jianzhi Zhang.

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Zhang, J., Zhang, Yp. & Rosenberg, H. Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30, 411–415 (2002). https://doi.org/10.1038/ng852

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