The genome of the green anole lizard and a comparative analysis with birds and mammals

Journal name:
Nature
Volume:
477,
Pages:
587–591
Date published:
DOI:
doi:10.1038/nature10390
Received
Accepted
Published online

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments1. Among amniotes, genome sequences are available for mammals and birds2, 3, 4, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes2. Also, A. carolinensis mobile elements are very young and diverse—more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds5. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

At a glance

Figures

  1. Amniote phylogeny based on protein synonymous sites showing major features of amniote evolution.
    Figure 1: Amniote phylogeny based on protein synonymous sites showing major features of amniote evolution.

    Major characteristics of lizard evolution including homogenization of GC content, high sex chromosome turnover and high levels of repeat insertion are featured. Sex chromosome inventions are indicated in red. Branch length is proportional to dS (the synonymous substitution rate); dS of each branch is indicated above the line.

  2. A. carolinensis-chicken synteny map reveals synteny of reptile microchromosomes but dissimilar GC and repeat content.
    Figure 2: A. carolinensis–chicken synteny map reveals synteny of reptile microchromosomes but dissimilar GC and repeat content.

    a, Very few rearrangements have occurred in the 280 million years since A. carolinensis and chicken diverged. A. carolinensis microchromosomes are exclusively syntenic to chicken microchromosomes. Horizontal coloured bars depict the six A. carolinensis macrochromosomes (1–6) and the six (of 12) A. carolinensis microchromosomes that have sequence anchored to them that is syntenic to the chicken genome (7, 8, 9, X, LGg, LGh). Chromosomes that could be ordered by size were assigned a number; the smaller microchromosomes that could not be distinguished by size were assigned a lowercase letter. Each colour corresponds to a different chicken chromosome as indicated in the key. Any part of an A. carolinensis chromosome that is syntenic to a chicken microchromosome is indicated by ‘m’. b, Chicken microchromosomes have both higher GC content and lower repeat content than chicken macrochromosomes, whereas A. carolinensis chromosomes do not vary in GC or repeat content by chromosome size. Large circles designate the GC percentage of each chromosome in the chicken and lizard genomes with greater than 100kb of sequence anchored to it. Small circles designate the percentage of the genome made up of repetitive sequence of each chromosome in the chicken (blue circles) and lizard (red circles) genomes.

  3. The A. carolinensis genome lacks isochores.
    Figure 3: The A. carolinensis genome lacks isochores.

    The A. carolinensis genome shows only very local variation in GC content, unlike the human and chicken genomes, which also show larger trends in GC variation, sometimes called isochores. Syntenic regions of human chromosome 14, chicken chromosome 5 and A. carolinensis chromosome 1 are shown. The human and chicken regions are inverted and rearranged to align with the A. carolinensis region. Blue lines depict GC percentage in 20-kb windows. The purple line designates the genome average. Green lines represent examples of syntenic anchors between the three genomes.

  4. The A. carolinensis genome contains a newly discovered X chromosome.
    Figure 4: The A. carolinensis genome contains a newly discovered X chromosome.

    a, b, The X chromosome, a microchromosome, is found in one copy in male A. carolinensis (a) and in two copies in females (b). The BAC 206M13 (CHORI-318 BAC library) is hybridized to the p arm of the X chromosome using FISH in both male and female metaphase spreads. 206M13 and ten other BACs showed this sex-specific pattern in cells derived from five male and five female individuals. Original magnification, ×1,000.

  5. A phylogeny of 93 Anolis species clarifies the biogeographic history of anoles.
    Figure 5: A phylogeny of 93 Anolis species clarifies the biogeographic history of anoles.

    Anolis ecomorphs derive from convergent evolution and not from frequent inter-island migration. Using conserved primer pairs distributed across the genome of A. carolinensis, we obtain sequences from 46 genomically diverse loci evolving at a range of evolutionary rates and representing both protein-coding and non-coding regions. Maximum likelihood analyses of this new data set of 20kb aligned nucleotides infer nearly all previously established anole relationships while also partially resolving the basal relationships that have plagued previous studies. Open circles indicate bootstrap (bs) values <70; grey-shaded circles, 70<bs<95; filled circles, bs >95.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

References

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Author information

  1. These authors contributed equally to this work.

    • Jessica Alföldi &
    • Federica Di Palma

Affiliations

  1. Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA

    • Jessica Alföldi,
    • Federica Di Palma,
    • Manfred Grabherr,
    • Evan Mauceli,
    • Pamela Russell,
    • Jacob D. Jaffe,
    • David Heiman,
    • Jeremy Johnson,
    • Marcia Lara,
    • Sally E. Peach,
    • Ross Swofford,
    • Jason Turner-Maier,
    • Sarah Young,
    • Eric S. Lander &
    • Kerstin Lindblad-Toh
  2. Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina 27606, USA

    • Christina Williams &
    • Matthew Breen
  3. MRC Functional Genomics Unit, University of Oxford, Department of Physiology, Anatomy and Genetics, Oxford OX1 3QX, UK

    • Lesheng Kong,
    • Matthew K. Fujita,
    • Andreas Heger &
    • Chris P. Ponting
  4. Stanford University School of Medicine, Department of Developmental Biology, Stanford, California 94305, USA

    • Craig B. Lowe
  5. University of Rochester, Rochester, New York 14607, USA

    • Richard E. Glor
  6. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, Mississippi 39762, USA

    • David A. Ray &
    • Jeremy D. Smith
  7. Department of Biology, Queens College, the City University of New York, New York, New York 11367, USA

    • Stephane Boissinot
  8. Biology Department and Graduate Program in Marine Genomics, College of Charleston, Charleston, South Carolina 29424, USA

    • Andrew M. Shedlock
  9. Harvard Medical School, Boston, Massachusetts 02115, USA

    • Christopher Botka
  10. Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado 80045, USA

    • Todd A. Castoe &
    • David D. Pollock
  11. The Center for Genomics and Bioinformatics, Indiana University, Bloomington, Indiana 47405, USA

    • John K. Colbourne &
    • Zachary Smith
  12. Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Matthew K. Fujita,
    • Ricardo Godinez Moreno,
    • Daniel E. Janes,
    • Chris L. Organ,
    • Thomas Sanger,
    • Scott V. Edwards &
    • Jonathan B. Losos
  13. Children’s Hospital Oakland Research Institute, Oakland, California 94609, USA

    • Boudewijn F. ten Hallers,
    • Pieter J. de Jong &
    • Maxim Y. Koriabine
  14. Center for Biomolecular Science and Engineering, University of California, Santa Cruz, California 95064, USA

    • David Haussler
  15. Department of Biological Sciences and Geology, Queensborough Community College, Bayside, New York 11364, USA

    • Peter A. Novick
  16. Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA

    • Steven Poe
  17. Program in Computational Bioscience, University of Colorado School of Medicine, Aurora, Colorado 80045, USA

    • David D. Pollock
  18. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia 20560, USA

    • Kevin de Queiroz
  19. Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK

    • Steve Searle &
    • Amonida Zadissa
  20. Departments of Psychology and Zoology, Program in Neuroscience, Michigan State University, East Lansing, Michigan 48824, USA

    • Juli Wade
  21. Department of Environmental Health Science and Georgia Genomics Facility, University of Georgia, Athens, Georgia 30602, USA

    • Travis C. Glenn
  22. Biology Department, Boston University, Boston, Massachusetts 02215, USA

    • Christopher J. Schneider
  23. Center for Comparative Medicine and Translational Research, North Carolina State University, Raleigh, North Carolina 27695, USA

    • Matthew Breen
  24. University of North Carolina Lineberger Comprehensive Cancer Center, Chapel Hill, North Carolina 27514, USA

    • Matthew Breen
  25. Science for Life Laboratory Uppsala, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala 751 23, Sweden

    • Kerstin Lindblad-Toh

Contributions

J.A., F.D. and K.L.-T. planned and oversaw the project. M.G., D. Heiman and S.Y. assembled the genome. B.F.t.H., M.Y.K. and P.J.d.J. constructed the BAC library. T.C.G. and J.W. provided tissues for sequencing libraries and FISH analysis. M.B., C.W. and D. Heiman anchored the genome. T.A.C. and D.D.P. assembled the mitochondrial genome. J.K.C. and Z.S. constructed the cDNA library. S.S. and A.Z. annotated the genome. L.K., A.H. and C.P.P. performed the gene repertoire analysis. T.S. aided egg protein experimental design. J.D.J. and S.E.P. performed egg mass spectrometry. M.G. performed genome synteny analysis. E.M. performed segmental duplication analysis. C.W. and M.B. discovered the sex chromosomes and the pericentromeric inversions. P.R. performed the microchromosome and GC analysis. M.K.F. and C.P.P. participated in microchromosome and GC data interpretation. D.A.R. constructed the repeat library. D.A.R., S.B., P.A.N., A.M.S., J.D.S. and C.B. performed the repeat analysis. M.G., J.B.L., R.E.G., S.P., K.d.Q. and R.S. participated in phylogeny data collection. R.E.G., S.P., K.d.Q. and R.S. participated in phylogeny analysis. All authors participated in data discussion and interpretation. J.A., F.D., C.B.L., R.G., D.A.R., S.V.E., C.J.S., J.B.L., E.S.L., M.B., C.P.P. and K.L.-T. wrote the paper with input from other authors.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

The A. carolinensis whole-genome shotgun project has been deposited in GenBank under the project accession AAWZ00000000.2. All phylogeny sequence data can be found at http://purl.org/phylo/treebase/phylows/study/TB2:S11713.

Author details

Supplementary information

PDF files

  1. Supplementary Information (4M)

    This file contains Supplementary Methods, Supplementary Notes, Supplementary Figures 1-10 with legends, Supplementary Tables 1-3, 8-13, and 15-20. See separate excel files for Supplementary Tables 4-7 and 14.

Excel files

  1. Supplementary Table 4 (238K)

    The table contains a translation table of NCBI scaffolds and accession numbers to Broad scaffold numbers.

  2. Supplementary Table 5 (44K)

    The table contains mapped BACs and their AnoCar 2.0 scaffold location.

  3. Supplementary Table 6 (92K)

    This table contains a detailed mapping of Chicken/Lizard synteny blocks.

  4. Supplementary Table 7 (509K)

    This table contains statistics on segmental duplication by chromosome.

  5. Supplementary Table 14 (175K)

    The table contains Proteins identified in A. carolinensis egg.

Additional data