Abstract
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.
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References
Losos J (2009) Lizards in an evolutionary tree. University of California Press, Berkeley, CA
Losos J, Jackman T, Larson A et al (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118
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 64:2731–2745
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 477:587–591
Gans C, Billet F, Maderson P (1985) Biology of the reptilia, vol 14. John Wiley & Sons, New York
Gans C, Billet F (1985) Biology of the Reptilia, vol 15. John Wiley & Sons, New York
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 269:129–137
Tschopp P, Sherratt E, Sanger TJ et al (2014) A relative shift in cloacal location repositions external genitalia in amniote evolution. Nature 516:391–394
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 281:20140329
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 35:107–119
Gamble T, Geneva A, Glor R, Zarkower D (2014) Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68:1027–1041
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 363:308–319
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 23:491–497
Koshiba-Takeuchi K, Mori A, Kaynak B et al (2009) Reptilian heart development and the molecular basis of cardiac chamber evolution. Nature 461:95–98
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 295:1596–1608
Gredler M, Sanger T, Cohn M (2015) Development of the cloaca, hemipenes, and hemiclitores in the green anole, Anolis carolinensis. Sex Dev 9:21–33
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 322:156–165
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 15:184
Butler MA, Sawyer SA, Losos JB (2007) Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447:202–205
Butler M, Losos J (2002) Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecol Monogr 72:541–559
Butler M, Schoener T, Losos J (2000) The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution 54:259–272
Sanger T, Sherratt E, McGlothlin J et al (2013) Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67:2180–2193
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 104:437–445
Johnson M, Wade J (2010) Behavioural display systems across nine Anolis lizard species: sexual dimorphisms in structure and function. Proc Biol Sci 277:1711–1719
Cox R, Stenquist D, Calsbeek R (2009) Testosterone, growth and the evolution of sexual size dimorphism. J Evol Biol 22:1586–1598
Losos J, Arnold S, Bejerano G et al (2013) Evolutionary biology for the 21st century. PLoS Biol 11:e1001466
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 279:739–748
Vavilov V (1922) The law of homologous series in variation. J Genet 12:47–89
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:e63651
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:e105004
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 17:339
Gredler M, Larkins C, Leal F et al (2014) Evolution of external genitalia: insights from reptilian development. Sex Dev 8:311–326
Sanger T, Gredler M, Cohn M (2015) Resurrecting embryos of the tuatara, Sphenodon punctatus, to resolve vertebrate phallus evolution. Biol Lett 11:20150694
Perriton C, Powles N, Chiang C et al (2002) Sonic hedgehog signaling from the urethral epithelium controls external genital development. Dev Biol 247:26–46
Gredler M, Seifert A, Cohn M (2015) Morphogenesis and patterning of the phallus and cloaca in the american alligator, Alligator mississippiensis. Sex Dev 9:53–67
Leal F, Cohn M (2015) Development of hemipenes in the ball python snake Python regius. Sex Dev 9:6–20
Larkins C, Cohn M (2015) Phallus development in the turtle Trachemys scripta. Sex Dev 9:34–42
Herrera A, Shuster S, Perriton C, Cohn M (2013) Developmental basis of phallus reduction during bird evolution. Curr Biol 23:1065–1074
Cohn M (2011) Development of the external genitalia: conserved and divergent mechanisms of appendage patterning. Dev Dyn 240:1108–1115
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 110:20651–20656
Tollis M, Hutchins E, Kusumi K (2014) Reptile genomes open the frontier for comparative analysis of amniote development and regeneration. Int J Dev Biol 58:863–871
Liu Y, Zhou Q, Wang Y et al (2015) Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration. Nat Commun 6:10033
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 4:45
Carroll S (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36
Gilles A, Averof M (2014) Functional genetics for all: engineered nucleases, CRISPR and the gene editing revolution. EvoDevo 5:43
Bassett A, Tibbit C, Ponting C, Liu J-L (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4:220–228
Nomura T, Yamashita W, Gotoh H, Ono K (2015) Genetic manipulation of reptilian embryos: toward an understanding of cortical development and evolution. Front Neurosci 9:45
Sanger T, Hime P, Johnson M et al (2008) Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herp Rev 39:58–63
Acknowledgments
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.
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Sanger, T.J., Kircher, B.K. (2017). Model Clades Versus Model Species: Anolis Lizards as an Integrative Model of Anatomical Evolution. In: Sheng, G. (eds) Avian and Reptilian Developmental Biology. Methods in Molecular Biology, vol 1650. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7216-6_19
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DOI: https://doi.org/10.1007/978-1-4939-7216-6_19
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