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

Volumn 62, Issue 8, 2008, Pages 2042-2064

  Brandley, Matthew C ^a   Huelsenbeck, John P ^a   Wiens, John J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Ancestral state reconstruction; Divergence time estimation; Evolutionary rate; Limb reduction; Macroevolution; Morphology; Phylogeny; Squamata

Indexed keywords

ANCESTRY; DIVERGENCE; EVOLUTIONARY BIOLOGY; LIMB; MORPHOLOGY; MORPHOMETRY; PERSISTENCE; PHYLOGENY; RECONSTRUCTION; REPTILE;

ALGORITHM; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CALIBRATION; ECOLOGY; EVOLUTION; GENETICS; LIMB; MOLECULAR EVOLUTION; MORPHOGENESIS; PHYLOGENY; PHYSIOLOGY; REGRESSION ANALYSIS; REPTILE; SPECIES DIFFERENTIATION; STATISTICAL MODEL; TIME;

ALGORITHMS; ANIMALS; BODY PATTERNING; CALIBRATION; ECOLOGY; EVOLUTION; EVOLUTION, MOLECULAR; EXTREMITIES; GENETIC SPECIATION; MODELS, GENETIC; MODELS, STATISTICAL; PHYLOGENY; REGRESSION ANALYSIS; REPTILES; TIME FACTORS;

REPTILIA; SQUAMATA;

EID: 47749133826     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00430.x     Document Type: Article

References (75)

1. Alberch, P., and E. Gale. 1985. A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution 39 : 8 23.
2. Bellairs, A. d'A. 1950. The limbs of snakes, with special reference to the hind limb rudiments of Trachyboa boulengeri. Br. J. Herpetol. 1 : 73 83.
3. Bruno, S., and S. Maugeri. 1976. Rettili d'Italia: Tartarughe e Sauri. I.A. Martello, Firenze, Italia.
4. Bull, J. J., and E. L. Charnov. 1985. On irreversible evolution. Evolution 39 : 1149 1155.
5. Caputo, V., B. Lanza, and R. Palmieri. 1995. Body elongation and limb reduction in the genus Chalcides Laurenti 1768 (Squamata Scincidae): a comparative study. Trop. Zool. 8 : 95 152.
6. Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2005. From DNA to diversity: molecular genetics and the evolution of animal design. 2nd edn. Blackwell Publishing, Malden, MA.
7. Choquenot, D., and A. E. Greer. 1987. Intrapopulational and interspecific variation in digital limb bones and presacral vertebrae of the genus Hemiergis (Lacertilia, Scincidae). J. Herpetol. 23 : 274 281.
8. Cogger, H. G. 1992. Reptiles and amphibians of Australia. 5th edn. Ralph Curtis Books, Hollywood, FL.
9. Cohn, M. J., and C. Tickle. 1999. Developmental basis of limblessness and axial regionalization in snakes. Nature 399 : 474 479.
10. Drummond, A. J., S. Y. H. Ho, M. J. Phillips, and A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLOS Biol. 4 : e88.
11. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17 : 368 376.
12. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125 : 1 15.
13. Fürbringer, M. 1870. Die knochen und muskeln der extremitäten bei den schlangenähnlichen sauriern. Vergleichend-anatomische Abhandlung. W. Engelmann, Leipzig, Germany.
14. Futuyma, D. J. 2005. Evolution. Sinauer Associates, Sunderland, MA.
15. Gans, C. 1975. Tetrapod limblessness: evolution and functional corollaries. Am. Zool. 15 : 455 467.
16. Gans, C., and J.-P. Gasc. 1990. Tests on the locomotion of the elongate and limbless reptile Ophisaurus apodus (Sauria: Anguidae). J. Zool. Lond. 222 : 517 536.
17. Garland, T., Jr., P. H. Harvey, and A. R. Ives 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41 : 18 32.
18. Gasc, J.-P., and C. Gans. 1990. Test on locomotion of the elongate and limbless lizard Anguis fragilis (Squamata: Anguidae). Copeia 1990 : 1055 1067.
19. Gingerich, P. D. 2001. Rates of evolution on the time scale of the evolutionary process. Genetica 112/113 : 127 144.
20. Gould, S. J. 1970. Dollo on Dollo's law: irreversibility and the status of evolutionary laws. J. Hist. Biol. 3 : 189 212.
21. Graur, D., and W. Martin. 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet. 20 : 80 86.
22. Greer, A. E. 1987. Limb reduction in the lizard genus Lerista. 1. Variation in the number of phalanges and presacral vertebrae. J. Herpetol. 21 : 267 276.
23. Greer, A. E. 1990. Limb reduction in the scincid lizard genus Lerista. 2. Variation in the bone complements of the front and rear limbs and the number of postsacral vertebrae. J. Herpetol. 24 : 142 150.
24. Greer, A. E. 1991. Limb reduction in squamates: identification of the lineages and discussion of the trends. J. Herpetol. 25 : 166 173.
25. Greer, A. E., and D. Choquenot. 1989. Intrapopulational and interspecific variation in digital limb bones and presacral vertebrae of the genus Hemiergis (Lacertilia, Scincidae). J. Herpetol. 23 : 274 281.
26. Greer, A. E., V. Caputo, B. Lanza, and R. Palmieri. 1998. Observations on limb reduction in the scincid lizard genus Chalcides. J. Herpetol. 32 : 244 252.
27. Hastings, W. K. 1970. Monte Carlo sampling methods using Markov chains and their applications. Biometrika 57 : 97 109.
28. Hendry, A. P., and M. T. Kinnison. 1999. The pace of modern life: measuring rates of microevolution. Evolution 53 : 1637 1653.
29. Hibbett, D. S. 2004. Trends in morphological evolution in Homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches. Syst. Biol. 53 : 889 903.
30. Huelsenbeck, J. P., R. Nielsen, and J. P. Bollback. 2003. Stochastic mapping of morphological characters. Syst. Biol. 52 : 131 158.
31. Hugall, A. F., R. Foster, and M. S. Y. Lee. 2007. Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Syst. Biol. 56 : 543 563.
32. Kearney, M. 2002. The appendicular skeleton in amphisbaenians. Copeia 2002 : 719 738.
33. Kearney, M., and B. L. Stuart. 2004. Repeated evolution of limblessness and digging heads in worm lizards revealed by DNA from old bones. Proc. R. Soc. Lond. B 271 : 1677 1683.
34. Kluge, A. G. 1976. Phylogenetic relationships in the lizard family Pygopodidae: an evaluation of theory, methods and data. Misc. Publ. Mus. Zool. Univ., Michigan 152. 72 Pp.
35. Kohlsdorf, T., and G. P. Wagner. 2006. Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata). Evolution 60 : 1896 1912.
36. Lande, R. 1978. Evolutionary mechanisms of limb loss in tetrapods. Evolution 32 : 73 92.
37. Larget, B., and D. L. Simon. 1999. Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol. Biol. Evol. 16 : 750 759.
38. Lewis, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50 : 913 925.
39. Lynch, M. 1990. The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136 : 727 741.
40. Marshall, C. R., E. C. Raff, and R. A. Raff. 1994. Dollo's law and the death and resurrection of genes. Proc. Natl. Acad. Sci. USA 91 : 12283 12287.
41. Martins, E. P. 2004. COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu. Department of Biology, Indiana Univ., Bloomington, IN.
42. Metropolis, N., A. W. Rosenbluth, M. N. Rosenbluth, A. H. Teller, and E. Teller. 1953. Equation of state calculations by fast computing machines. J. Chem. Phys. 21 : 1087 1092.
43. Mlynarski, M., and Z. Madej. 1961. The rudimentary limbs in Aniliidae (Serpentes). Br. J. Herpetol. 3 : 1 6.
44. Murphy, J. B., D. G. Barker, and B. W. Tryon. 1978. Miscellaneous notes on the reproductive biology of reptiles. 11. Eleven species of the family Boidae, genera Candoia, Corallus, Epicrates and Python. J. Herpetol. 12 : 385 390.
45. Oakley, T. H., and C. W. Cunningham. 2000. Independent contrasts succeed where explicit ancestor reconstructions fail in a known bacteriophage phylogeny. Evolution 54 : 397 405.
46. Ord, T. J., and E. P. Martins. 2006. Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Anim. Behav. 71 : 1411 1429.
47. Orsini, J.-P., and M. Cheylan. 1981. Chalcides chalcides (Linnaeus 1758) - Erzschleiche. Pp. 318 337. in W. Böhme, ed., Handbuch der Reptilien und Amphibien Europas. Vol. 1. Akademische Verlagsgesellschaft, Wiesbaden, Germany.
48. Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255 : 37 45.
49. Pagel, M., and F. Lutzoni. 2002. Accounting for phylogenetic uncertainty in comparative studies of evolution and adaptation. Pp. 148 161 in M. Lässig and A. Valleriani, eds., Biological evolution and statistical physics. Springer-Verlag, Berlin, Germany.
50. Pough, F. H., R. M. Andrews, J. E. Cadle, M. L. Crump, A. H. Savitzky, and K. D. Wells. 2004. Herpetology. 3rd edn. Prentice-Hall, Upper Saddle River, NJ.
51. Presch, W. 1975. The evolution of limb reduction in the teiid lizard genus Bachia. Bull. S. Cal. Acad. Sci. 74 : 113 121.
52. Pulquério, M. J. F., and R. A. Nichols. 2007. Dates from the molecular clock: how wrong can we be? Trends Ecol. Evol. 22 : 180 184.
53. Renous, S., and J. P. Gasc. 1979. Etude des modalités de reduction des members chez un squamate serpentiform: Scelotes, scincidé afro-malagache. Ann. Sci. Nat. Ser. 13 : 99 132.
54. Renous, S., E. Höfling, and J-P Gasc. 1995. Analysis of the locomotion pattern of two microteiid lizards with reduced limbs, Calyptommatus leiolepis and Nothobachia ablephara (Gymnophthalmidae). Zoology 99 : 21 38.
55. Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43 : 223 225.
56. Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19 : 101 109.
57. Sanderson, M. J. 2003. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19 : 301 302.
58. Schultz, T. R., R. B. Cocroft, and G. A. Churchill. 1996. The reconstruction of ancestral character states. Evolution 50 : 504 511.
59. Sewertzoff, A. N. 1931. Morphologische gesetzmässigkeiten der evolution. Gustav Fischer, Jena, Germany.
60. Shapiro, M. D. 2002. Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony. J. Morphol. 254 : 211 231.
61. Shapiro, M. D., J. Hanken, and N. Rosenthal. 2003. Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis. J. Exp. Zool. B (Mol. Dev. Evol.) 297B : 48 56.
62. Stokely, P. S. 1947. Limblessness and correlated changes in the girdles of a comparative morphological series of lizards. Am. Mid. Nat. 38 : 725 754.
63. Thorne, J. L., and H. Kishino. 2002. Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 51 : 689 702.
64. Tierney, L. 1996. Introduction to general state-space Markov chain theory. Pp. 59 74 in W. R. S. Gilks, S. Richardson, and D. J. Spiegelhalter, eds., Markov Chain Monte Carlo in Practice. Chapman and Hall, London, England.
65. Uetz, P. 2007. The reptile database. http://www.reptile-database.org. Accessed September 8, 2007.
66. Verdinelli, I., and L. Wasserman. 1995. Computer Bayes factors using a generalization of the Savage-Dickey density ratio. J. Am. Stat. Assoc. 90 : 614 618.
67. Vidal, N., and S. B. Hedges. 2005. The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C. R. Biol. 328 : 1000 1008.
68. Wagner, G. P. 1982. The logical structure of irreversible systems-transformations: a theorem concerning Dollo's law and chaotic movement. J. Theor. Biol. 96 : 337 346.
69. Wagner, G. P. 2005. The developmental evolution of avian digit homology: an update. Theor. Biosci. 124 : 165 183.
70. Walton, M., B. C. Jayne, and A. F. Bennett. 1990. The energetic cost of limbless locomotion. Science 249 : 524 528.
71. Whiting, A. S., A. M. Bauer, and J. W. Sites, Jr. 2003. Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata:Scincidae). Mol. Phylogenet. Evol. 29 : 582 598.
72. Wiens, J. J., and J. L. Slingluff. 2001. How lizards turn into snakes: a phylogenetic analysis of body-form evolution in anguid lizards. Evolution 55 : 2303 2318.
73. Wiens, J. J., M. C. Brandley, and T. W. Reeder. 2006. Why does a trait evolve multiple times within a clade? Repeated evolution of snake-like body form in squamate reptiles. Evolution 60 : 123 141.
74. Wiens, J. J., C. A. Kuczynski, W. E. Duellman, and T. W. Reeder. 2007. Loss and re-evolution of complex life cycles in marsupial frogs: can ancestral trait reconstruction mislead? Evolution 61 : 1886 1899.
75. Zangerl, R. 1945. Contributions to the osteology of the post-cranial skeleton of the Amphisbaenidae. Am. Midl. Nat. 33 : 764 780.