Hand/foot splitting and the 're-evolution' of mesopodial skeletal elements during the evolution and radiation of chameleons

BMC Evolutionary Biology

Volumn 15, Issue 1, 2015, Pages

  Diaz, Raul E ^a,b   Trainor, Paul A ^c,d  

^a LA SIERRA UNIVERSITY   (United States)

^b NATURAL HISTORY MUSEUM OF LOS ANGELES COUNTY   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE RADIATION; AVIFAUNA; BODY SIZE; CLADISTICS; COMPARATIVE STUDY; DIVERGENCE; EVOLUTION; EVOLUTIONARY BIOLOGY; HYBRIDIZATION; IN SITU TEST; LIMB; LIZARD; MORPHOGENESIS; RODENT; SKELETON;

AMNIOTA; AMPHIBIA; CHAMAELEO CALYPTRATUS; CHAMAELEONIDAE; RODENTIA;

ANATOMY AND HISTOLOGY; ANIMAL; CLASSIFICATION; ECOSYSTEM; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; LIZARD; MORPHOGENESIS; PHYLOGENY; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; EXTREMITIES; LIZARDS; MORPHOGENESIS; PHYLOGENY;

EID: 84941919478     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-015-0464-4     Document Type: Article

References (94)

1. Sahni N, Yi S, Zhong Q, Jailkhani N, Charloteaux B, Cusick ME, et al. Edgotype: a fundamental link between genotype and phenotype. Curr Opin Genet Dev. 2013;23:649-57.
2. Sandell LL, Julianella A, Melton KR, Lynn M, Walker M, Inman KE, et al. A phenotype-driven ENU mutagenesis screen identifies novel alleles with functional roles in early mouse craniofacial development. Genesis. 2011;49(4):342-59.
3. Beddington R. Mouse mutagenesis: from gene to phenotype and back again. Curr Biol. 1998;8:R840-2.
4. Shearin AL, Ostrander EA. Canine Morphology: hunting for genes and tracking mutations. PLoS Biol. 2010;8(3):e1000310.
5. Niswander L. Limb mutants: what can they tell us about normal limb development? Curr Opin Genet Dev. 1997;7(4):530-6.
6. Wilkie AOM. Why study human limb malformations? J Anatomy. 2003;202(1):27-35.
7. Wagner GP. Homology, Genes and Evolutionary Innovation. Princeton: University Press; 2014.
8. Darwin C. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. London: John Murray; 1859.
9. Shubin N, Tabin C, Carroll S. Fossils, genes and the evolution of animal limbs. Nature. 1997;388(6643):639-48.
10. Hall BK. Fins into limbs: Evolution, Development and Transformation. Chicago: University of Chicago Press; 2007.
11. Clack JA. Gaining ground: the origin and evolution of tetrapods (life of the past). 2nd ed. Indiana: University Press; 2012.
12. Zeller R, López-Ríos J, Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet. 2009;10:845-58.
13. Cooper KL, Sears KE, Uygur A, Maier J, Baczkowski KS, Brosnahan M, et al. Patterning and post-patterning modes of evolutionary digit loss. Nature. 2014;511(7507):41-5.
14. Lopez-Rios J, Duchesne A, Speziale D, Andrey G, Peterson KA, Germann P, et al. Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs. Nature. 2014;511(7507):46-51.
15. De Bakker MA, Fowler DA, den Oude K, Dondorp EM, Nevas MC, Horbanczuk JO, et al. Digit loss in archosaur evolution and the interplay between selection and constraints. Nature. 2013;500(7463):445-8.
16. Sears KE, Bormet AK, Rockwell A, Powers LE, Noelle Cooper L, Wheeler MB. Developmental basis of mammalian digit reduction: a case study in pigs. Evol Dev. 2011;13(6):533-41.
17. Young RL, Caputo V, Giovannotti M, Kohlsdorf T, Vargas AO, May GE, et al. Evolution of digit identity in the three-toed Italian skink Chalcides chalcides: a new case of digit identity frame shift. Evol Dev. 2009;11(6):647-58.
18. Shapiro MD, Hanken J, Rosenthal N. Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. J Exp Zool B Mol Dev Evol. 2003;297B:48-56.
19. Shapiro MD. Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony. J Morphol. 2002;254(3):211-31.
20. Greer AE. 1991. Limb reduction in squamates: identification of the lineages and discussion of the trends. J Herpetol. 1991;25:166-73.
21. Tolley KA, Herrel A. The Biology of Chameleons. California: University of California Press; 2013.
22. Tilbury C. Chameleons of Africa, an Atlas including the chameleons of Europe. the Middle East and Asia: Edition Chimaira; 2010.
23. nd Edition. Frankfurt, Germany: Edition Chimaria; 2004.
24. Hurle JM, Garcia-Martinez V, Ganan Y, Climent V, Blasco M. Morphogenesis of the prehensile autopodium in the common chameleon (Chamaeleo chamaeleo). J Morphol. 1987;194(2):187-94.
25. Rieppel O. Studies on skeleton formation in reptiles II. Chamaeleo hoehnelii (Squamata: Chamaeleonidae), with comments on the homology of carpal and tarsal bones. Herpetologica. 1993;49:66-78.
26. Tabin CJ. Why we have (only) five fingers per hand: Hox genes and the evolution of paired limbs. Development. 1992;116:289-96.
27. Diaz Jr RE, Anderson CV, Baumann D, Jewell D, Kupronis R, Piraquive C, et al. Captive care, raising and breeding of the Veiled Chameleon, Chamaeleo calyptratus. In press A. Emerging Model Organisms. Cold Spring Harbor Lab Publishers.
28. Diaz Jr RE, Anderson CV, Baumann D, Jewell D, Kupronis R, Piraquive C, et al. The Veiled Chameleon, Chamaeleo calyptratus Duméril and Duméril 1851: A model for studying reptile bodyplan development and evolution. In press B. Emerging Model Organisms. Cold Spring Harbor Lab Publishers.
29. Stower MJ, Diaz RE, Fernandez LC, Crother MW, Crother B, Marco A, et al. Bi-modal strategy of gastrulation in reptiles. Dev Dyn. doi: 10.1002/dvdy.24300.
30. Sandell LL, Kurosaka H, Trainor PA. Whole mount nuclear fluorescent imaging: Convenient documentation of embryo morphology. Genesis. 2012; 50 (1) DOI: 10.1002/dvg.22344.
31. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature. 1995;375(6534):787-90.
32. Walker MB, Kimmel CB. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech Histochem. 2007;82(1):23-8.
33. Dujif PH, van Bokhoven H, Brunner HG. Pathogenesis of split-hand/split-foot malformation. Hum Mol Genet. 2003;12:R51-60.
34. Naruse T, Takahara M, Takagi M, Oberg KC, Ogino T. Dev Growth Differ. 2007;49(6):533-41.
35. Oberg KC, Feenstra JC, Manske PR, Tonkin MA. 2010. Developmental biology and classification of congenital anomalies of the hand and upper extremity. J Hand Surg Am. 2010;35(12):2066-76.
36. Sun X, Mariani FV, Martin GR. Functions of FGF signaling from the apical ectodermal ridge in limb development. Nature. 2002;418(6897):501-8.
37. Verheyden JM, Sun X. An FGF/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature. 2008;454(7204):638-41.
38. Greer AE. Hyperphalangy in squamates: insight on the reacquisition of primitive character states in limb-reduced lineages. J Herpetol. 1992;26:327-9.
39. Greer AE, Smith S. Aspects of the morphology and reproductive biology of the Australian earless dragon lizard Tympanocryptis tetraporophora. Aust Zool. 1999;31:55-70.
40. Mariani FV, Ahn CP, Martin GR. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature. 2008;453(7193):401-5.
41. Saunders JW. The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J Exp Zool. 1948;108:363-404.
42. Hernandez-Martinez R, Covarrubias L. Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev Growth Differ. 2011;53(2):245-58.
43. Diaz-Hernandez ME, Rios-Flores AJ, Abarca-Buis RF, Bustamante M, Chimal-Monroy J. Molecular control of interdigital cell death and cell differentiation by Retinoic Acid during digit development. J Dev Biol. 2014;2:138-57.
44. Weatherbee SD, Behringer RR, Rasweiler JJ, Niswander LA. Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification. Proc Natl Acad Sci USA. 2006;103(41):15103-7.
45. Merino R, Rodriguez-Leon J, Macias D, Gañan Y, Economides EN, Hurle JM. The BMP antagonist Gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb. Development. 1999;126(23):5515-22.
46. Zou H, Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 1996;272(5262):738-41.
47. Zuzarte-Luis V, Hurle JM. Programmed cell death in the developing limb. Int J Dev Biol. 2002;46:871-6.
48. Milaire J, Rooze M. Hereditary and induced modifications of the normal necrotic patterns in the developing limb buds of the rat and mouse: facts and hypothesis. Arch Biol. 1983;94:459-90.
49. Ahn K, Mishina Y, Hanks MC, Behringer RR, Crenshaw EB. BMPR-IA signaling is required for the formation of the apical ectodermal ridge and dorsal-ventral patterning of the limb. Development. 2001;128(22):350-62.
50. Zuniga A, Haramis AP, McMahon AP, Zeller R. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature. 1999;401(6753):598-602.
51. Zuniga A, Michos O, Spitz F, Haramis AP, Panman L, Galli A, et al. Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev. 2004;18(13):1553-64.
52. Pajni-Underwood S, Wilson CP, Elder C, Mishina Y, Lewandoski M. BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling. Development. 2007;134(12):2359-68.
53. Chen Y, Zhao X. Shaping limbs by apoptosis. J Exp Zool. 1998;282(6):691-702.
54. Hogan BL. Bone morphogenetic proteins in development. Curr Opin Genet Dev. 1996;6(4):432-8.
55. Zuzarte-Luis V, Hurle JM. Programmed cell death in the embryonic vertebrate limb. Semin Cell Dev Biol. 2005;16(2):261-9.
56. Guha U, Gomes WA, Kobayashi T, Pestell RG, Kessler JA. In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb. Dev Biol. 2002;249(1):108-20.
57. Hernandez-Martinez R, Castro-Obregon S, Covarrubias L. Progressive interdigital cell death: regulation by the antagonistic interaction between fibroblast growth factor 8 and retinoic acid. Development. 2009;136(21):3669-78.
58. Norrie JL, Lewandowski JP, Bouldin CM, Amarnath S, Li Q, Vokes MS, et al. Dynamics of BMP signaling in limb bud mesenchyme and polydactyly. Dev Biol. 2014;393(2):270-81.
59. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol. 2008;4(1):33-41.
60. Hall BK. Bones and Cartilage: developmental and evolutionary skeletal biology. Academic Press. 2006.
61. Gegenbauer C. Zur morphologie der gliedmassen der wirbeltiere. Morph Jahrb. 1876;II:396-420.
62. Schaeffer B. The morphological and functional evolution of the tarsus in amphibians and reptiles. Bull Am Mus Nat Hist. 1941; 78:395-472.
63. Shubin NH, Alberch P. A morphogenetic approach to the origin and basic organization of the tetrapod skeleton. Evol Biol. 1986;20:319-87.
64. Fabrezi M, Abdala V, Oliver MIM. Developmental basis of limb homology in lizards. Anat Rec. 2007;290:900-12.
65. Leal F, Tarazona OA, Ramirez-Pinilla MP. Limb development in the gekkonid lizard Gonatodes albogularis: a reconsideration of homology in the lizard carpus and tarsus. J Morphol. 2010;271(11):1328-41.
66. Tolley KA, Townsend TM, Vences M. Large-scale phylogeny of chameleons suggests African origins and Eocence diversification. Proc R Soc Lond B Biol Sci. 2013;280:20130184.
67. Botelho JF, Ossa-Fuentes L, Soto-Acuna S, Smith-Paredes D, Nunes-Leon D, Salinas-Saavedra M, et al. New developmental evidence clarifies the Evolution of wrist bones in the Dinosaur-Bird transition. PLoS Biol. 2014;12(9), e1001957.
68. Solem RC, Eames BF, Tokita M, Schneider RA. Mesenchymal and mechanical mechanisms of secondary cartilage induction. Dev Biol. 2011;356(1):28-39.
69. Glaw F, Hawlitschek O, Ruthensteiner B. A new genus name for an ancient Malagasy chameleon clade and a PDF-embedded 3D model of its skeleton. Salamandra. 2013;49:237-8.
70. Glaw F, Kohler J, Townsend TM, Vences M. Rivaling the world's smallest reptiles: discovery of miniaturized and microendemic new species of leaf chameleons (Brookesia) from Northern Madagascar. PLoS One. 2012;7(2), e31314.
71. Riedel J, Bohme W, Bleckmann H, Spinner M. Microornamentation of leaf chameleons (Chamaeleonidae: Brookesia, Rhampholeon, and Rieppeleon) - with comments on the evolution of microstructure in the chamaeleonidae. J Morphol. 2014;276(2):167-84.
72. Renous-Lécuru S. Morphologie compare du carpe chez les Lepidosauriens actuels (Rhynchocephales, Lacertiliens, Amphisbeniens). Morphol Jb. 1973;119:727-66.
73. Sjögren SJ. Die entwicklung des handund hand-und fuss-skelets bei Chamaeleo bitaeniatus ellioti. Morphol Jb. 1940;41(85):243-60.
74. Estes R, Pregill G. Phylogenetic relationships of the lizard families. Stanford, California: Stanford University Press; 1988.
75. Armstrong T, Chaffin D. Some biomechanical aspects of the carpal tunnel. J Biomech. 1979;12(7):567-70.
76. Rieppel O, Crumly C. Paedomorphosis and skull structure in Malagasy chamaeleons (Reptilia: Chamaeleoninae). J Zool. 1997;243:351-80.
77. Hanken J, Wake DB. Miniaturization of body size: organismal consequences and evolutionary significance. Annu Rev Ecol Evol Syst. 1993;24:501-19.
78. Hanken J, Wake DB. Biology of tiny animals: systematics of the minute salamanders (Thorius: Plethodontidae) from Veracruz and Puebla, Mexico, with descriptions of five new species. Copeia. 1998;1998:312-45.
79. Wake DB, Wake MH, Specht CD. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science. 2011;331:1032-5.
80. Zhu J, Nakamura E, Nguyen MT, Bao X, Akiyama H, Mackem S. Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev Cell. 2008;14(4):624-32.
81. DeLisle AM, Fischer L, Tuan RS. Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage. 2000;8(5):309-34.
82. Hall BK, Miyake T. All for one and one for all: condensations and the initiation of skeletal development. Bioessays. 2000;22(2):138-47.
83. Kohlsdorf T, Wagner GP. Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata). Evolution. 2006;60(9):1896-912.
84. Galis F, Arntzen JW, Lande R. Dollo's law and the irreversibility of digit loss in Bachia. Evolution. 2010;64(8):2466-76.
85. Brandley MC, Huelsenbeck JP, Wiens JJ. Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution. 2008;62:2042-64.
86. Siler CD, Diesmos AC, Alcala AC, Brown RM. Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification. Mol Phylogenet Evol. 2011;59(1):53-65.
87. Grismer LL, Huat EQS, Siler CD, Onn CK, Wood Jr PL, Grismer JL, et al. Peninsular Malaysia's first limbless lizard: a new species of skink of the genus Larutia (Böhme) from Pulau Pinang with a phylogeny of the genus. Zootaxa. 2011;2799:29-40.
88. Metscher BD. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histochemical resolution. Dev Dyn. 2009;238(3):632-40.
89. Lekevicius E. Vacant niches in nature, ecology, and evolutionary theory: a mini-review. Ekologija. 2009;55(3-4):165-74.
90. Chew KY, Shaw G, Yu H, Pask AJ, Renfree MB. Heterochrony in the regulation of the developing marsupial limb. Dev Dyn. 2014;243(2):324-38.
91. Uetz P, Hošek J. The Reptile Database, http://www.reptile-database.org, accessed Jan 8, 2014.
92. O'Keefe FR, Sidor CA, Larsson HCE, Maga A, Ide O. Evolution and homology of the Astragalus in early amniotes: new fossils, new perspectives. J Morphol. 2006;267:415-25.
93. Peabody F. The origin of the astragalus of reptiles. Evolution. 1951;5:339-44.
94. Romer AS, Parsons T. Vertebrate Body. Philadelphia, Pennsylvania USA: WB Saunders Company; 1977.