Convergent evolution of the genomes of marine mammals

Journal name:
Nature Genetics
Volume:
47,
Pages:
272–275
Year published:
DOI:
doi:10.1038/ng.3198
Received
Accepted
Published online

Marine mammals from different mammalian orders share several phenotypic traits adapted to the aquatic environment and therefore represent a classic example of convergent evolution. To investigate convergent evolution at the genomic level, we sequenced and performed de novo assembly of the genomes of three species of marine mammals (the killer whale, walrus and manatee) from three mammalian orders that share independently evolved phenotypic adaptations to a marine existence. Our comparative genomic analyses found that convergent amino acid substitutions were widespread throughout the genome and that a subset of these substitutions were in genes evolving under positive selection and putatively associated with a marine phenotype. However, we found higher levels of convergent amino acid substitutions in a control set of terrestrial sister taxa to the marine mammals. Our results suggest that, whereas convergent molecular evolution is relatively common, adaptive molecular convergence linked to phenotypic convergence is comparatively rare.

At a glance

Figures

  1. Phylogeny of 20 eutherian mammalian genome sequences, rooted with a marsupial outgroup.
    Figure 1: Phylogeny of 20 eutherian mammalian genome sequences, rooted with a marsupial outgroup.

    Branches representing the independent evolution of marine mammal lineages, for which tests for positive selection and parallel nonsynonymous amino acid substitutions were performed, are colored red. Branches of the control set of terrestrial taxa, for which tests for positive selection and parallel nonsynonymous amino acid substitutions were also performed, are colored black. Marine mammal illustrations are by Uko Gorter.

  2. Genome scans for convergence.
    Figure 2: Genome scans for convergence.

    Marine mammal genomes showed a large number of parallel substitutions (blue) that occurred along the branches of at least two marine mammal lineages since they evolved from a terrestrial ancestor. Parallel substitutions that occurred in positively selected genes are shaded red.

  3. Glutathione pathway (KEGG pathway map 00480).
    Supplementary Fig. 1: Glutathione pathway (KEGG pathway map 00480).

    Solid lines indicate direct relationships between enzymes and metabolites, and dashed lines indicate that more than one step is involved in a process. Genes are shown in rectangles. ANPEP highlighted in green was one of only five genes found evolving under positive selection along the combined marine mammal branch after correcting for multiple testing. GCLC highlighted in red was found to be evolving under positive selection along the combined marine mammal branch and the walrus branch and contained a convergent substitution shared by all three marine mammal lineages. GGT6 highlighted in bold font was found to be evolving under positive selection along the walrus branch. Yim et al.11 previously found evidence for GSR evolving under positive selection in the bottlenose dolphin and experimentally demonstrated the importance of glutathione as an antioxidant in cetacean cells during hypoxic or oxidative stress, e.g., during deep or long dives. This figure is adapted from Figure 3a of Yim et al.11.

  4. Percentage of convergent substitutions for all pairwise comparisons among all 14 species in the phylogeny.
    Supplementary Fig. 2: Percentage of convergent substitutions for all pairwise comparisons among all 14 species in the phylogeny.

    The dashed line indicates the average.

  5. Pie charts of genome fractions as identified by RepeatMasker.
    Supplementary Fig. 3: Pie charts of genome fractions as identified by RepeatMasker.

    (a) Killer whale. (b) Bottlenose dolphin. (c) Manatee. (d) Walrus.

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Author information

  1. These authors contributed equally to this work.

    • Andrew D Foote,
    • Yue Liu,
    • Gregg W C Thomas &
    • Tomáš Vinař

Affiliations

  1. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.

    • Andrew D Foote &
    • M Thomas P Gilbert
  2. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

    • Andrew D Foote,
    • Nagarjun Vijay &
    • Jochen B W Wolf
  3. Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas, USA.

    • Yue Liu,
    • Jixin Deng,
    • Shannon Dugan,
    • Vandita Joshi,
    • Ziad Khan,
    • Christie Kovar,
    • Sandra L Lee,
    • Xiang Qin,
    • Jiaxin Qu,
    • Donna M Muzny,
    • Kim C Worley &
    • Richard A Gibbs
  4. School of Informatics and Computing, Indiana University, Bloomington, Indiana, USA.

    • Gregg W C Thomas &
    • Matthew W Hahn
  5. Faculty of Mathematics, Physics and Informatics, Comenius University, Bratislava, Slovakia.

    • Tomáš Vinař
  6. Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA.

    • Jessica Alföldi &
    • Kerstin Lindblad-Toh
  7. Dolfinarium Harderwijk, Harderwijk, the Netherlands.

    • Cornelis E van Elk
  8. Sirenia Project, Southeast Ecological Science Center, US Geological Survey, Gainesville, Florida, USA.

    • Margaret E Hunter
  9. Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

    • Kerstin Lindblad-Toh &
    • Jochen B W Wolf
  10. Marine Biomedicine and Environmental Science Center, Medical University of South Carolina, Charleston, South Carolina, USA.

    • Annalaura Mancia
  11. Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.

    • Annalaura Mancia
  12. Center for Theoretical Evolutionary Genomics, University of California, Berkeley, Berkeley, California, USA.

    • Rasmus Nielsen
  13. Center for Biomolecular Science and Engineering, University of California, Santa Cruz, Santa Cruz, California, USA.

    • Brian J Raney
  14. Department of Biology, Indiana University, Bloomington, Indiana, USA.

    • Matthew W Hahn
  15. Trace and Environmental DNA Laboratory, Department of Environment and Agriculture, Curtin University, Perth, Western Australia, Australia.

    • M Thomas P Gilbert

Contributions

A.D.F. and M.T.P.G. coordinated the analyses and wrote the manuscript. K.C.W. led the sequencing consortium project. Genome assembly: Y.L., J.D., J.Q. and K.C.W. (lead). Sequencing project managers: V.J. and S.D. Sequencing: Z.K., C.K. and D.M.M. (lead). Sequencing libraries and quality control: S.L.L. RNA sequencing analysis: X.Q. Manatee genome sequencing project: K.L.-T. and J.A. Tissue samples for dolphin: A.M. Tissue samples for walrus and killer whale: C.E.v.E. Tissue samples for manatee: M.E.H. DNA and RNA extraction (killer whale and walrus): A.D.F. Multi-genome alignment: B.J.R. Generation of ortholog set, likelihood ratio testing and GO analyses: T.V. Convergence testing: M.W.H. and G.W.C.T. Experimental design, bioinformatics and statistical support: R.N., N.V. and J.B.W.W. Additional manuscript preparation: B.J.R., M.W.H., R.A.G., N.V., T.V., J.B.W.W. and K.C.W. Principal investigators: R.A.G. and M.T.P.G.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

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Author details

Supplementary information

Supplementary Figures

  1. Supplementary Figure 1: Glutathione pathway (KEGG pathway map 00480). (73 KB)

    Solid lines indicate direct relationships between enzymes and metabolites, and dashed lines indicate that more than one step is involved in a process. Genes are shown in rectangles. ANPEP highlighted in green was one of only five genes found evolving under positive selection along the combined marine mammal branch after correcting for multiple testing. GCLC highlighted in red was found to be evolving under positive selection along the combined marine mammal branch and the walrus branch and contained a convergent substitution shared by all three marine mammal lineages. GGT6 highlighted in bold font was found to be evolving under positive selection along the walrus branch. Yim et al.11 previously found evidence for GSR evolving under positive selection in the bottlenose dolphin and experimentally demonstrated the importance of glutathione as an antioxidant in cetacean cells during hypoxic or oxidative stress, e.g., during deep or long dives. This figure is adapted from Figure 3a of Yim et al.11.

  2. Supplementary Figure 2: Percentage of convergent substitutions for all pairwise comparisons among all 14 species in the phylogeny. (27 KB)

    The dashed line indicates the average.

  3. Supplementary Figure 3: Pie charts of genome fractions as identified by RepeatMasker. (58 KB)

    (a) Killer whale. (b) Bottlenose dolphin. (c) Manatee. (d) Walrus.

PDF files

  1. Supplementary Text and Figures (1,064 KB)

    Supplementary Figures 1–3 and Supplementary Tables 1, 2, 4–6, 8 and 14.

Excel files

  1. Supplementary Table 3 (62 KB)

    Genes identified as evolving under positive selection along the combined marine mammal branch.

  2. Supplementary Table 7 (48 KB)

    Positively selected genes that contain non-identical or 'common' amino acid substitutions at the same residue in all three marine mammal lineages.

  3. Supplementary Table 9 (44 KB)

    Genes identified as evolving under positive selection along the cetacean branch.

  4. Supplementary Table 10 (79 KB)

    Genes identified as evolving under positive selection along the sirenian (manatee) branch.

  5. Supplementary Table 11 (86 KB)

    Genes identified as evolving under positive selection along the pinniped (walrus) branch.

  6. Supplementary Table 12 (55 KB)

    Functional enrichment analysis of positively selected genes along the combined marine mammal branch.

  7. Supplementary Table 13 (53 KB)

    Significant shifts in gene ontology categories along the combined marine mammal branch.

Additional data