Model Clades Versus Model Species: Anolis Lizards as an Integrative Model of Anatomical Evolution

  • Thomas J. SangerEmail author
  • Bonnie K. Kircher
Part of the Methods in Molecular Biology book series (MIMB, volume 1650)


Anolis lizards, known for their replicated patterns of morphological diversification, are widely studied in the fields of evolution and ecology. As a textbook example of adaptive radiation, this genus has supported decades of intense study in natural history, behavior, morphological evolution, and systematics. Following the publication of the A. carolinensis genome, research on Anolis lizards has expanded into new areas, toward obtaining an understanding the developmental and genetic bases of anole diversity. Here, we discuss recent progress in these areas and the burgeoning methodological toolkit that has been used to elucidate the genetic mechanisms underlying anatomical variation in this group. We also highlight the growing number of studies that have used A. carolinensis as the representative squamate in large-scale comparison of amniote evolution and development. Finally, we address one of the largest technical challenges biologists are facing in making Anolis a model for integrative studies of ecology, evolution, development, and genetics, the development of ex-ovo culturing techniques that have broad utility. Ultimately, with the power to ask questions across all biological scales in this diverse genus full, anoles are rapidly becoming a uniquely integrative and powerful biological system.

Key words

Eco-evo-devo Evolution Macroevolution Dimorphism 



We would like to thank P. Tschopp, R. Diaz, and M. Cohn for valuable discussion on the culturing protocols discussed herein. R. Dale supplied us with the bleaching protocol based on his work on zebrafish. This chapter is supported by laboratory start-up funds from Loyola University in Chicago to T.J.S. and an NSF Graduate Research Fellowship to B.K.K.


  1. 1.
    Losos J (2009) Lizards in an evolutionary tree. University of California Press, Berkeley, CAGoogle Scholar
  2. 2.
    Losos J, Jackman T, Larson A et al (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118CrossRefPubMedGoogle Scholar
  3. 3.
    Mahler D, Revell L, Glor R, Losos J (2010) Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean Anoles. Evolution 64:2731–2745CrossRefPubMedGoogle Scholar
  4. 4.
    Alföldi J, Di Palma F, Grabherr M et al (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587–591CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Gans C, Billet F, Maderson P (1985) Biology of the reptilia, vol 14. John Wiley & Sons, New YorkGoogle Scholar
  6. 6.
    Gans C, Billet F (1985) Biology of the Reptilia, vol 15. John Wiley & Sons, New YorkGoogle Scholar
  7. 7.
    Sanger T, Losos J, Gibson-Brown J (2008) A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. J Morphol 269:129–137CrossRefPubMedGoogle Scholar
  8. 8.
    Tschopp P, Sherratt E, Sanger TJ et al (2014) A relative shift in cloacal location repositions external genitalia in amniote evolution. Nature 516:391–394CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Sanger T, Seav S, Tokita M et al (2014) The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards. Proc Biol Sci 281:20140329CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Infante C, Mihala A, Park S et al (2015) Shared enhancer activity in the limbs and phallus and functional divergence of a limb-genital cis-regulatory element in snakes. Dev Cell 35:107–119CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gamble T, Geneva A, Glor R, Zarkower D (2014) Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68:1027–1041CrossRefPubMedGoogle Scholar
  12. 12.
    Eckalbar W, Lasku E, Infante C et al (2012) Somitogenesis in the anole lizard and alligator reveals evolutionary convergence and divergence in the amniote segmentation clock. Dev Biol 363:308–319CrossRefPubMedGoogle Scholar
  13. 13.
    Kusumi K, May C, Eckalbar W (2013) A large-scale view of the evolution of amniote development: insights from somitogenesis in reptiles. Curr Opin Genet Dev 23:491–497CrossRefPubMedGoogle Scholar
  14. 14.
    Koshiba-Takeuchi K, Mori A, Kaynak B et al (2009) Reptilian heart development and the molecular basis of cardiac chamber evolution. Nature 461:95–98CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ritzman T, Stroik L, Julik E et al (2012) The gross anatomy of the original and regenerated tail in the green anole (Anolis carolinensis). Anat Rec 295:1596–1608CrossRefGoogle Scholar
  16. 16.
    Gredler M, Sanger T, Cohn M (2015) Development of the cloaca, hemipenes, and hemiclitores in the green anole, Anolis carolinensis. Sex Dev 9:21–33CrossRefPubMedGoogle Scholar
  17. 17.
    Park S, Infante C, Rivera-Davila L, Menke D (2014) Conserved regulation of hoxc11 by pitx1 in Anolis lizards. J Exp Zool B Mol Dev Evol 322:156–165CrossRefPubMedGoogle Scholar
  18. 18.
    Diaz R, Trainor P (2015) Hand/foot splitting and the “re-evolution” of mesopodial skeletal elements during the evolution and radiation of chameleons. BMC Evol Biol 15:184CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Butler MA, Sawyer SA, Losos JB (2007) Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447:202–205CrossRefPubMedGoogle Scholar
  20. 20.
    Butler M, Losos J (2002) Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecol Monogr 72:541–559CrossRefGoogle Scholar
  21. 21.
    Butler M, Schoener T, Losos J (2000) The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution 54:259–272PubMedGoogle Scholar
  22. 22.
    Sanger T, Sherratt E, McGlothlin J et al (2013) Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67:2180–2193CrossRefPubMedGoogle Scholar
  23. 23.
    Johnson M, Cohen R, Vandecar J, Wade J (2011) Relationships among reproductive morphology, behavior, and testosterone in a natural population of green anole lizards. Physiol Behav 104:437–445CrossRefPubMedGoogle Scholar
  24. 24.
    Johnson M, Wade J (2010) Behavioural display systems across nine Anolis lizard species: sexual dimorphisms in structure and function. Proc Biol Sci 277:1711–1719CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Cox R, Stenquist D, Calsbeek R (2009) Testosterone, growth and the evolution of sexual size dimorphism. J Evol Biol 22:1586–1598CrossRefPubMedGoogle Scholar
  26. 26.
    Losos J, Arnold S, Bejerano G et al (2013) Evolutionary biology for the 21st century. PLoS Biol 11:e1001466CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Sanger T, Revell L, Gibson-Brown J, Losos J (2012) Repeated modification of early limb morphogenesis programmes underlies the convergence of relative limb length in Anolis lizards. Proc R Soc B Biol Sci 279:739–748CrossRefGoogle Scholar
  28. 28.
    Vavilov V (1922) The law of homologous series in variation. J Genet 12:47–89CrossRefGoogle Scholar
  29. 29.
    Jensen B, van den Berg G, van den Doel R et al (2013) Development of the hearts of lizards and snakes and perspectives to cardiac evolution. PLoS One 8:e63651CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hutchins E, Markov G, Eckalbar W et al (2014) Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. PLoS One 9:e105004CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hutchins E, Eckalbar W, Wolter J et al (2016) Differential expression of conserved and novel microRNAs during tail regeneration in the lizard Anolis carolinensis. BMC Genomics 17:339CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Gredler M, Larkins C, Leal F et al (2014) Evolution of external genitalia: insights from reptilian development. Sex Dev 8:311–326CrossRefPubMedGoogle Scholar
  33. 33.
    Sanger T, Gredler M, Cohn M (2015) Resurrecting embryos of the tuatara, Sphenodon punctatus, to resolve vertebrate phallus evolution. Biol Lett 11:20150694CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Perriton C, Powles N, Chiang C et al (2002) Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26–46CrossRefPubMedGoogle Scholar
  35. 35.
    Gredler M, Seifert A, Cohn M (2015) Morphogenesis and patterning of the phallus and cloaca in the american alligator, Alligator mississippiensis. Sex Dev 9:53–67CrossRefPubMedGoogle Scholar
  36. 36.
    Leal F, Cohn M (2015) Development of hemipenes in the ball python snake Python regius. Sex Dev 9:6–20CrossRefPubMedGoogle Scholar
  37. 37.
    Larkins C, Cohn M (2015) Phallus development in the turtle Trachemys scripta. Sex Dev 9:34–42CrossRefPubMedGoogle Scholar
  38. 38.
    Herrera A, Shuster S, Perriton C, Cohn M (2013) Developmental basis of phallus reduction during bird evolution. Curr Biol 23:1065–1074CrossRefPubMedGoogle Scholar
  39. 39.
    Cohn M (2011) Development of the external genitalia: conserved and divergent mechanisms of appendage patterning. Dev Dyn 240:1108–1115CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Vonk F, Casewell N, Henkel C et al (2013) The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A 110:20651–20656CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Tollis M, Hutchins E, Kusumi K (2014) Reptile genomes open the frontier for comparative analysis of amniote development and regeneration. Int J Dev Biol 58:863–871CrossRefPubMedGoogle Scholar
  42. 42.
    Liu Y, Zhou Q, Wang Y et al (2015) Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration. Nat Commun 6:10033CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Georges A, Li Q, Lian J et al (2015) High-coverage sequencing and annotated assembly of the genome of the Australian dragon lizard Pogona vitticeps. Gigascience 4:45CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Carroll S (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36CrossRefPubMedGoogle Scholar
  45. 45.
    Gilles A, Averof M (2014) Functional genetics for all: engineered nucleases, CRISPR and the gene editing revolution. EvoDevo 5:43CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Bassett A, Tibbit C, Ponting C, Liu J-L (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4:220–228CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Nomura T, Yamashita W, Gotoh H, Ono K (2015) Genetic manipulation of reptilian embryos: toward an understanding of cortical development and evolution. Front Neurosci 9:45CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Sanger T, Hime P, Johnson M et al (2008) Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herp Rev 39:58–63Google Scholar

Copyright information

© Springer Science+Business Media LLC 2017

Authors and Affiliations

  1. 1.Department of BiologyLoyola University ChicagoChicagoUSA
  2. 2.Department of BiologyUniversity of FloridaGainesvilleUSA

Personalised recommendations