Evolutionary Biology

, Volume 41, Issue 4, pp 528–545 | Cite as

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

  • Emma Sherratt
  • David J. Gower
  • Christian Peter Klingenberg
  • Mark Wilkinson
Research Article


Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.


Caecilian Geometric morphometrics Macroevolution Micro computed tomography Tempo and mode 

Supplementary material

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Supplementary material 1 (DOCX 515 kb)
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Supplementary material 2 (XLS 122 kb)


  1. Adams, D. C., Berns, C. M., Kozak, K. H., & Wiens, J. J. (2009). Are rates of species diversification correlated with rates of morphological evolution? Proceedings of the Royal Society B Biological Sciences, 276(1668), 2729–2738.PubMedCentralGoogle Scholar
  2. Adams, D. C., Otarola-Castillo, E., & Sherratt, E. (2014). Geomorph: Software for geometric morphometric analyses. R package version 2.0. http://www.cran.r-project.org/web/packages/geomorph/index.html.
  3. Agarwal, I., Wilkinson, M., Mohapatra, P. P., Dutta, S. K., Giri, V. B., & Gower, D. J. (2013). The first teresomatan caecilian (Amphibia: Gymnophiona) from the Eastern Ghats of India—a new species of Gegeneophis Peters, 1880. Zootaxa, 3693(4), 534.Google Scholar
  4. AmphibiaWeb: Information on amphibian biology and conservation [web application] (2014). Berkeley, California: AmphibiaWeb. http://amphibiaweb.org/. Accessed 1 May 2014.
  5. Angielczyk, K. D., & Ruta, M. (2012). The roots of amphibian morphospace: A geometric morphometric analysis of Paleozoic temnospondyls. Fieldiana Life and Earth Sciences, 5, 40–58.Google Scholar
  6. Beaulieu, J. M., Ree, R. H., Cavender-Bares, J., Weiblen, G. D., & Donoghue, M. J. (2012). Synthesizing phylogenetic knowledge for ecological research. Ecology, 93(sp8), S4–S13.Google Scholar
  7. Bookstein, F. L. (1996). Biometrics, biomathematics and the morphometric synthesis. Bulletin of Mathematical Biology, 58(2), 313–365.PubMedGoogle Scholar
  8. Breuker, C. J., Debat, V., & Klingenberg, C. P. (2006). Functional evo-devo. Trends in Ecology & Evolution, 21, 488–492.Google Scholar
  9. Brooks, D. R., & McLennan, D. A. (1991). Phylogeny, ecology, and behaviour: a research program in comparative biology (p. 434). Chicago: The University of Chicago Press.Google Scholar
  10. Brusatte, S. L., Sakamoto, M., Montanari, S., & Harcourt Smith, W. E. H. (2012). The evolution of cranial form and function in theropod dinosaurs: Insights from geometric morphometrics. Journal of Evolutionary Biology, 25(2), 365–377.PubMedGoogle Scholar
  11. Burger, M., Branch, W. R., & Channing, A. (2004). Amphibians and reptiles of Monts Doudou, Gabon: species turnover along an elevational gradient. In B. L. Fisher (Ed.), Monts Doudou, Gabon: A floral and faunal inventory with reference to elevational variation (pp. 145–186). San Francisco: California Academy of Sciences.Google Scholar
  12. Casanovas-Vilar, I., & van Dam, J. (2013). Conservatism and adaptability during squirrel radiation: What is mandible shape telling us? PLoS ONE, 8(4), e61298.PubMedCentralPubMedGoogle Scholar
  13. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36(3), 499–516.Google Scholar
  14. Ciampaglio, C. N., Kemp, M., & McShea, D. W. (2001). Detecting changes in morphospace occupation patterns in the fossil record: Characterization and analysis of measures of disparity. Paleobiology, 27, 695–715.Google Scholar
  15. Clabaut, C., Bunje, P. M. E., Salzburger, W., & Meyer, A. (2007). Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution, 61(3), 560–578.PubMedGoogle Scholar
  16. Cooper, W. J., Parsons, K., McIntyre, A., Kern, B., McGee-Moore, A., & Albertson, R. C. (2010). Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLoS ONE, 5(3), e9551.PubMedCentralPubMedGoogle Scholar
  17. Dornburg, A., Sidlauskas, B., Santini, F., Sorenson, L., Near, T. J., & Alfaro, M. E. (2011). The influence of an innovative locomotor strategy on the phenoptypic diversification of triggerfishes (Family: Balistidae). Evolution, 65(7), 1912–1926.PubMedGoogle Scholar
  18. Drake, A. G., & Klingenberg, C. P. (2010). Large-scale diversification of skull shape in domestic dogs: Disparity and modularity. American Naturalist, 175(3), 289–301.PubMedGoogle Scholar
  19. Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis (p. 376). Chichester: Wiley.Google Scholar
  20. Ducey, P. K., Formanowicz, D. R., Boyet, L., Mailloux, J., & Nussbaum, R. (1993). Experimental examination of burrowing behavior in caecilians (Amphibia: Gymnophiona): Effects of soil compaction on burrowing ability of four species. Herpetologica, 49(4), 450–457.Google Scholar
  21. Eldredge, N., & Gould, S. J. (1972). Models in paleobiology. In T. J. M. Schopf (Ed.), Advances in Morphometrics (pp. 82–115). San Francisco: Freeman, Cooper & Co.Google Scholar
  22. Erwin, D. H. (2007). Disparity: Morphological pattern and developmental context. Palaeontology, 50, 57–73.Google Scholar
  23. Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125(1), 1–15.Google Scholar
  24. Felsenstein, J. (1988). Phylogenies and quantitative characters. Annual Review of Ecology and Systematics, 19, 455–471.Google Scholar
  25. Felsenstein, J. (2004). Inferring phylogenies (p. 664). Sunderland: Sinauer Associates, Inc.Google Scholar
  26. Figueirido, B., Serrano-Alarcón, F. J., Slater, G. J., & Palmqvist, P. (2010). Shape at the cross-roads: Homoplasy and history in the evolution of the carnivoran skull towards herbivory. Journal of Evolutionary Biology, 23(12), 2579–2594.PubMedGoogle Scholar
  27. Fortuny, J., Marcé-Nogué, J., De Esteban-Trivigno, S., Gil, L., & Galobart, À. (2011). Temnospondyli bite club: Ecomorphological patterns of the most diverse group of early tetrapods. Journal of Evolutionary Biology, 24(9), 2040–2054.PubMedGoogle Scholar
  28. Friedman, M. (2010). Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proceedings of the Royal Society of London, B Biological Sciences, 277, 1675–1683.Google Scholar
  29. Gans, C. (1974). Biomechanics: an approach to vertebrate biology (p. 272). Michigan: The University of Michigan Press.Google Scholar
  30. Gans, C. (1994). Approaches to the evolution of limbless locomotion. Cuadernos de Herpetología, 8, 12–17.Google Scholar
  31. Garland, T, Jr, & Ives, A. R. (2000). Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods. The American Naturalist, 155(3), 346–364.Google Scholar
  32. Gomes, A. D., Navas, C. A., Jared, C., Antoniazzi, M. M., Ceballos, N. R., & Moreira, R. G. (2013). Metabolic and endocrine changes during the reproductive cycle of dermatophagic caecilians in captivity. Zoology, 116, 277.PubMedGoogle Scholar
  33. Gower, D. J., Kupfer, A., Oommen, O. V., Himstedt, W., Nussbaum, R. A., Loader, S. P., et al. (2002). A molecular phylogeny of ichthyophiid caecilians (Amphibia: Gymnophiona: Ichthyophiidae): Out of India or out of South East Asia? Proceedings of the Royal Society B Biological Sciences, 269(1500), 1563–1569.PubMedCentralGoogle Scholar
  34. Gower, D. J., Loader, S. P., Moncrieff, C. B., & Wilkinson, M. (2004). Niche separation and comparative abundance of Boulengerula boulengeri and Scolecomorphus vittatus (Amphibia: Gymnophiona) in an East Usambara forest Tanzania. African Journal of Herpetology, 53(2), 183–190.Google Scholar
  35. Gower, D. J., San Mauro, D., Giri, V., Bhatta, G., Venu, G., Ramachandran, K., et al. (2011). Molecular systematics of caeciliid caecilians (Amphibia: Gymnophiona) of the Western Ghats India. Molecular Phylogenetics and Evolution, 59(3), 698–707.PubMedGoogle Scholar
  36. Gower, D. J., & Wilkinson, M. (2008). Caecilians (Gymnophiona). In: S. N. Stuart, M. Hoffmann, J. S. Chanson, N. A. Cox, R. Berridge,P. Ramani, et al. (Eds.), Threatened Amphibians of the World: Lynx Ediciones, with IUCN - The World Conservation Union, Conservation International, and Nature Serve (pp. 19-20), Barcelona.Google Scholar
  37. Gower, D. J., & Wilkinson, M. (2009). Caecilians (Gymnophiona) (pp. 369–372). The Timetree of Life: Oxford University Press.Google Scholar
  38. Gower, D. J., Wilkinson, M., Sherratt, E., & Kok, P. J. R. (2010). A new species of Rhinatrema Dumeril & Bibron (Amphibia: Gymnophiona: Rhinatrematidae) from Guyana. Zootaxa, 2391, 47–60.Google Scholar
  39. Harmon, L. J., Losos, J. B., Davies, T. J., Gillespie, R. G., Gittleman, J. L., Jennings, W. B., et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64, 2385–2396.PubMedGoogle Scholar
  40. Herrel, A., & Measey, G. J. (2010). The kinematics of locomotion in caecilians: Effects of substrate and body shape. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 313A(5), 301–309.Google Scholar
  41. Hoogmoed, M. S., Maciel, A. O., & Coragem, J. T. (2011). Discovery of the largest lungless tetrapod, Atretochoana eiselti (Taylor, 1968) (Amphibia: Gymnophiona: Typhlonectidae), in its natural habitat in Brazilian Amazonia Boletim do Museu Paraense Emílio Goeldi. Série Ciências Naturais, 6(3), 241–262.Google Scholar
  42. Kamei, R. G., Gower, D. J., Wilkinson, M., & Biju, S. D. (2013). Systematics of the caecilian family Chikilidae (Amphibia: Gymnophiona) with the description of three new species of Chikila from northeast India. Zootaxa, 3666(4), 401.Google Scholar
  43. Kamei, R. G., San Mauro, D., Gower, D. J., Van Bocxlaer, I., Sherratt, E., Thomas, A., et al. (2012). Discovery of a new family of amphibians from northeast India with ancient links to Africa. Proceedings of the Royal Society B Biological Sciences, 279(1737), 2396–2401.PubMedCentralGoogle Scholar
  44. Kimmel, C. B., Sidlauskas, B., & Clack, J. A. (2009). Linked morphological changes during palate evolution in early tetrapods. Journal of Anatomy, 215, 91–109.PubMedCentralPubMedGoogle Scholar
  45. Kleinteich, T., Maddin, H. C., Herzen, J., Beckmann, F., & Summers, A. P. (2012). Is solid always best? Cranial performance in solid and fenestrated caecilian skulls. Journal of Experimental Biology, 215, 833–844.PubMedGoogle Scholar
  46. Klingenberg, C. P. (1996). Multivariate allometry. In L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor, & D. E. Slice (Eds.), Advances in Morphometrics (pp. 23–49). New York: Plenum Press.Google Scholar
  47. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology Evolution and Systematics, 39, 115–132.Google Scholar
  48. Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635.PubMedGoogle Scholar
  49. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.PubMedGoogle Scholar
  50. Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56(10), 1909–1920.PubMedGoogle Scholar
  51. Klingenberg, C. P., Duttke, S., Whelan, S., & Kim, M. (2012). Developmental plasticity, morphological variation and evolvability: A multilevel analysis of morphometric integration in the shape of compound leaves. Journal of Evolutionary Biology, 25(1), 115–129.PubMedGoogle Scholar
  52. Klingenberg, C. P., & Ekau, W. (1996). A combined morphometric and phylogenetic analysis of an ecomorphological trend: Pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biological Journal of the Linnean Society, 59(2), 143–177.Google Scholar
  53. Klingenberg, C. P., & Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology, 59(3), 245–261.PubMedGoogle Scholar
  54. Klingenberg, C. P., & Marugán-Lobón, J. (2013). Evolutionary covariation in geometric morphometric data: Analyzing integration, modularity and allometry in a phylogenetic context. Systematic Biology, 62, 591–610.PubMedGoogle Scholar
  55. Kuehnel, S., & Kupfer, A. (2012). Sperm storage in caecilian amphibians. Frontiers in Zoology, 9(1), 12.PubMedCentralPubMedGoogle Scholar
  56. Kupfer, A. (2009). Sexual size dimorphism in caecilian amphibians analysis, review and directions for future research. Zoology, 112(5), 362–369.PubMedGoogle Scholar
  57. Kupfer, A., Gaucher, P., Wilkinson, M., & Gower, D. J. (2006a). Passive trapping of aquatic caecilians (Amphibia: Gynmophiona: Typhlonectidae). Studies on Neotropical Fauna and Environment, 41(2), 93–96.Google Scholar
  58. Kupfer, A., Müller, H., Antoniazzi, M. M., Jared, C., Greven, H., Nussbaum, R. A., et al. (2006b). Parental investment by skin feeding in a caecilian amphibian. Nature, 440(7086), 926–929.PubMedGoogle Scholar
  59. Kupfer, A., Nabhitabhata, J., & Himstedt, W. (2005). Life history of amphibians in the seasonal tropics: Habitat, community and population ecology of a caecilian (genus Ichthyophis). Journal of Zoology, 266(03), 237–247.Google Scholar
  60. Loader, S. P. (2005). Systematics and biogeography of amphibians of the African Eastern Arc mountains. Ph.D. Thesis, University of Glasgow, Glasgow, UK.Google Scholar
  61. Loader, S., Wilkinson, M., Cotton, J., Müller, H., Menegon, M., Howell, K. M., et al. (2011). Molecular phylogenetics of Boulengerula (Amphibia: Gymnophiona: Caeciliidae) and implications for taxonomy, biogeography and conservation. Herpetological Journal, 21(1), 5–16.Google Scholar
  62. Losos, J. B. (2009). Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Oakland: University of California Press.Google Scholar
  63. Maciel, A. O., & Hoogmoed, M. S. (2013). A new species of Microcaecilia (Amphibia: Gymnophiona: Siphonopidae) from the Guianan region of Brazil. Zootaxa, 3693(3), 387.Google Scholar
  64. Maddin, H. C., Jenkins, F. A, Jr, & Anderson, J. S. (2012a). The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of caecilians. PLoS ONE, 7(12), e50743.PubMedCentralPubMedGoogle Scholar
  65. Maddin, H. C., Russell, A. P., & Anderson, J. S. (2012b). Phylogenetic implications of the morphology of the braincase of caecilian amphibians (Gymnophiona). Zoological Journal of the Linnean Society, 166(1), 160–201.Google Scholar
  66. Maddison, W. P. (1991). Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Systematic Zoology, 40(3), 304–314.Google Scholar
  67. Marcus, L. F., Hingst-Zaher, E., & Zaher, H. (2000). Application of landmark morphometrics to skulls representing the orders of living mammals. Hystrix, 11(1), 27–47.Google Scholar
  68. Mattila, T. M., & Bokma, F. (2008). Extant mammal body masses suggest punctuated equilibrium. Proceedings of the Royal Society B Biological Sciences, 275(1648), 2195–2199.PubMedCentralGoogle Scholar
  69. McArdle, B. H., & Rodrigo, A. G. (1994). Estimating the ancestral states of a continuous-valued character using squared-change parsimony: An analytical solution. Systematic Biology, 43, 573–578.Google Scholar
  70. McKenna, M. F., Cranford, T. W., & Berta, A. (2003). Defining the odontocete melon: Comparisons using morphometric analysis. Integrative and Comparative Biology, 43(6), 931.Google Scholar
  71. Measey, G. J., Gower, D. J., Oommen, O. V., & Wilkinson, M. (2004). A subterranean generalist predator: Diet of the fossorial caecilian Gegeneophis ramaswamii (Amphibia; Gymnophiona; Caeciliidae) in southern India. Comptes Rendus Biologies, 327, 65–76.PubMedGoogle Scholar
  72. Meloro, C., & Jones, M. E. H. (2012). Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent ‘living fossil’ label. Journal of Evolutionary Biology, 25(11), 2194–2209.PubMedGoogle Scholar
  73. Meyer, A. (1993). Phylogenetic relationships and evoutionary processes in East African Cichlid fishes. Trends in Ecology & Evolution, 8(8), 279–284.Google Scholar
  74. Mohun, S. M., & Wilkinson, M. (2014). The eye of the caecilian Rhinatrema bivittatum (Amphibia: Gymnophiona: Rhinatrematidae). Acta Zoologica. doi:10.1111/azo.12061.
  75. Monteiro, L. R. (1999). Multivariate regression models and geometric morphometrics: The search for causal factors in the analysis of shape. Systematic Biology, 48(1), 192–199.PubMedGoogle Scholar
  76. Monteiro, L. R. (2013). Morphometrics and the comparative method: Studying the evolution of biological shape. Hystrix, 24(1), 25–32.Google Scholar
  77. Monteiro, L., & Nogueira, M. (2011). Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Evolutionary Biology, 11(1), 137.PubMedCentralPubMedGoogle Scholar
  78. Moodie, G. E. E. (1978). Observations on the life history of the caecilian Typhlonectes compressicaudus (Dumeril and Bibron) in the Amazon basin. Canadian Journal of Zoology, 56(4), 1005–1008.Google Scholar
  79. Müller, H. (2006a). Ontogeny of the skull, lower jaw, and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliidae) revisited. Journal of Morphology, 267, 968–986.PubMedGoogle Scholar
  80. Müller, H. (2006b). Ontogeny of the skull, lower jaw, and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliiidae) revisited. Journal of Morphology, 267, 968–986.PubMedGoogle Scholar
  81. Müller, H., Oommen, O., & Bartsch, P. (2005). Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). Zoomorphology, 124(4), 171–188.Google Scholar
  82. Müller, H., Wilkinson, M., Loader, S. P., Wirkner, C. S., & Gower, D. J. (2009). Morphology and function of the head in foetal and juvenile Scolecomorphus kirkii (Amphibia: Gymnophiona: Scolecomorphidae). Biological Journal of the Linnean Society, 96(3), 491–504.Google Scholar
  83. Neige, P. (2003). Spatial patterns of disparity and diversity of the recent cuttlefishes (Cephalopoda) across the Old World. Journal of Biogeography, 30(8), 1125–1137.Google Scholar
  84. Nevo, E. (1979). Adaptive convergence and divergence of subterranean mammals. Annual Review of Ecology and Systematics, 10, 269–308.Google Scholar
  85. Nicola, P. A., Monteiro, L. R., Pessoa, L. M., Von Zuben, F. J., Rohlf, F. J., & Dos Reis, S. F. (2003). Congruence of hierarchical, localized variation in cranial shape and molecular phylogenetic structure in spiny rats, genus Trinomys (Rodentia: Echimyidae). Biological Journal of the Linnean Society, 80(3), 385–396.Google Scholar
  86. Nishikawa, K., Matsui, M., Sudin, A., & Wong, A. (2013). A new striped Ichthyophis (Amphibia: Gymnophiona) from Mt. Kinabalu, Sabah, Malaysia. Current Herpetology, 32(2), 159–169.Google Scholar
  87. Nishikawa, K., Matsui, M., Yong, H.-S., Ahmad, N., Yambun, P., Belabut, D. M., et al. (2012). Molecular phylogeny and biogeography of caecilians from Southeast Asia (Amphibia, Gymnophiona, Ichthyophiidae), with special reference to high cryptic species diversity in Sundaland. Molecular Phylogenetics and Evolution, 63(3), 714–723.PubMedGoogle Scholar
  88. Nogueira, M. R., Peracchi, A. L., & Monteiro, L. R. (2009). Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Functional Ecology, 23(4), 715–723.Google Scholar
  89. Nussbaum, R. A. (1983). The evolution of a unique dual jaw-closing mechanism in caecilians: (Amphibia: Gymnophiona) and its bearing on caecilian ancestry. Journal of Zoology, 199(4), 545–554.Google Scholar
  90. Nussbaum, R. A. (1985). Systematics of caecilians (Amphibia: Gymnophiona) of the family Scolecomorphidae. Occasional Papers of the Museum of Zoology University of Michigan, 713, 1–52.Google Scholar
  91. Nussbaum, R., & Gans, C. (1980). On the Ichthyophis (Amphibia: Gymnophiona) of Sri Lanka. Spolia Zeylanica, 35, 137–154.Google Scholar
  92. Nussbaum, R. A., & Pfrender, M. E. (1998). Revision of the African caecilian genus Schistometopum Parker (Amphibia: Gymnophiona: Caeciliidae). Miscellaneous Publications Museum of Zoology University of Michigan, 187, 1–48.Google Scholar
  93. Nussbaum, R. A., & Wilkinson, M. (1989). On the classification and phylogeny of caecilians (Amphibia: Gymnophiona), a critical review. Herpetological Monographs, 3, 1–42.Google Scholar
  94. Nussbaum, R. A., & Wilkinson, M. (1995). A new genus of lungless tetrapod: A radically divergent caecilian (Amphibia: Gymnophiona). Proceedings of the Royal Society B Biological Sciences, 261(1362), 331–335.Google Scholar
  95. Olson, M. E. (2012). The developmental renaissance in adaptationism. Trends in Ecology & Evolution, 27(5), 278–287.Google Scholar
  96. Olson, E. C., & Miller, R. L. (1958). Morphological integration (p. 376). Chicago: University of Chicago Press.Google Scholar
  97. Oommen, O. V., Measey, G. J., Gower, D. J., & Wilkinson, M. (2000). Distribution and abundance of the caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona) in southern Kerala. Current Science, 79(9), 1386–1389.Google Scholar
  98. Pagel, M., Venditti, C., & Meade, A. (2006). Large punctuational contribution of speciation to evolutionary divergence at the molecular level. Science, 314(5796), 119–121.PubMedGoogle Scholar
  99. Pennell, M. W., & Harmon, L. J. (2013). An integrative view of phylogenetic comparative methods: connections to population genetics, community ecology, and paleobiology. Annals of the New York Academy of Sciences, 1289(1), 90–105.PubMedGoogle Scholar
  100. Pie, M. R., & Weitz, J. S. (2005). A null model for morphospace occupation. American Naturalist, 166, E1–E13.PubMedGoogle Scholar
  101. Pierce, S. E., Angielczyk, K. D., & Rayfield, E. J. (2008). Patterns of morphospace occupation and mechanical performance in extant crocodilian skulls: A combined geometric morphometric and finite element modeling approach. Journal of Morphology, 269(7), 840–864.PubMedGoogle Scholar
  102. Pipan, T., & Culver, D. C. (2012). Convergence and divergence in the subterranean realm: A reassessment. Biological Journal of the Linnean Society, 107(1), 1–14.Google Scholar
  103. Prevosti, F. J., Turazzini, G. F., Ercoli, M. D., & Hingst-Zaher, E. (2012). Mandible shape in marsupial and placental carnivorous mammals: A morphological comparative study using geometric morphometrics. Zoological Journal of the Linnean Society, 164, 836–855.Google Scholar
  104. Price, S. A., Holzman, R., Near, T. J., & Wainwright, P. C. (2011). Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecology Letters, 14(5), 462–469.PubMedGoogle Scholar
  105. Purvis, A. (2004). Evolution: How do characters evolve? Nature, 432(7014), 165.Google Scholar
  106. R Development Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria.Google Scholar
  107. Rabosky, D. L., & Adams, D. C. (2012). Rates of morphological evolution are correlated with species richness in salamanders. Evolution, 66(6), 1807–1818.PubMedGoogle Scholar
  108. Renous, S. (1990). Morphologie cranienne d’un Siphonopidé américain, Microcaecilian unicolor (Amphibien, Gymnophione) et interprétation fonctionnelle. Gegenbaurs Morphologisches Jahrbuch, 136(6), 781–806.PubMedGoogle Scholar
  109. Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63, 3258–3268.PubMedGoogle Scholar
  110. Ricklefs, R. E. (2004). Cladogenesis and morphological diversification in passerine birds. Nature, 430(6997), 338–341.PubMedGoogle Scholar
  111. Roelants, K., Gower, D. J., Wilkinson, M., Loader, S. P., Biju, S. D., Guillaume, K., et al. (2007). Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences, 104(3), 887–892.Google Scholar
  112. Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55(11), 2143–2160.PubMedGoogle Scholar
  113. Rohlf, F. J. (2002). Geometric morphometrics and phylogeny. In N. MacLeod & P. L. Forey (Eds.), Morphology, shape and phylogeny (pp. 175–193). London: Francis & Taylor.Google Scholar
  114. Sakamoto, M., & Ruta, M. (2012). Convergence and divergence in the evolution of cat skulls: Temporal and spatial patterns of morphological diversity. PLoS ONE, 7(7), e39752.PubMedCentralPubMedGoogle Scholar
  115. Sallan, L. C., & Friedman, M. (2012). Heads or tails: Staged diversification in vertebrate evolutionary radiations. Proceedings of the Royal Society of London, B Biological Sciences, 279, 2025–2032.Google Scholar
  116. San Mauro D. (2010). A multilocus timescale for the origin of extant amphibians. Molecular Phylogenetics and Evolution, 56(2), 554–561.Google Scholar
  117. San Mauro D, Gower, D. J., Müller, H., Loader, S. P., Zardoya, R., Nussbaum, R. A., et al. (2014). Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Molecular Phylogenetics and Evolution, 73, 177–189. doi:10.1016/j.ympev.2014.01.009.
  118. San Mauro, D., Gower, D. J., Oommen, O. V., Wilkinson, M., & Zardoya, R. (2004). Phylogeny of caecilian amphibians (Gymnophiona) based on complete mitochondrial genomes and nuclear RAG1. Molecular Phylogenetics and Evolution, 33(2), 413–427.PubMedGoogle Scholar
  119. Sanger, T. J., Mahler, D. L., Abzhanov, A., & Losos, J. B. (2012). Roles for modularity and constraint in the evolution of cranial diversity among Anolis lizards. Evolution, 66(5), 1525–1542.PubMedGoogle Scholar
  120. Schluter, D. (2000). The ecology of adaptive radiation (p. 296). Oxford: Oxford Uviversity Press.Google Scholar
  121. Sidlauskas, B. (2008). Continuous and arrested morphological diversification in sister clades of characiform fishes: A phylomorphospace approach. Evolution, 62(12), 3135–3156.PubMedGoogle Scholar
  122. Sidlauskas, B. L., Mol, J. H., & Vari, R. P. (2011). Dealing with allometry in linear and geometric morphometrics: A taxonomic case study in the Leporinus cylindriformis group (Characiformes: Anostomidae) with description of a new species from Suriname. Zoological Journal of the Linnean Society, 162, 103–130.Google Scholar
  123. Simpson, G. G. (1944). Tempo and mode in evolution. New York: Columbia University Press.Google Scholar
  124. Stayton, C. T. (2003). Functional and morphological evolution of herbivory in lizards. Integrative and Comparative Biology, 43(6), 913.Google Scholar
  125. Stayton, C. T. (2005). Morphological evolution of the lizard skull: A geometric morphometrics survey. Journal of Morphology, 263(1), 47–59.PubMedGoogle Scholar
  126. Stayton, C. T. (2011). Biomechanics on the half shell: Functional performance influences patterns of morphological variation in the emydid turtle carapace. Zoology, 114, 213–223.PubMedGoogle Scholar
  127. Stayton, C. T., & Ruta, M. (2006). Geometric morphometrics of the skull roof of stereospondyls (Amphibia: Temnospondyli). Palaeontology, 49, 307–337.Google Scholar
  128. Streelman, T. J., & Danley, P. D. (2003). The stages of vertebrate evolutionary radiation. Trends in Ecology & Evolution, 18(3), 126–131.Google Scholar
  129. Taylor, E. H. (1968). The caecilians of the world: a taxonomic review (p. 848). Lawrence: University of Kansas Press.Google Scholar
  130. Taylor, E. H. (1969). Skulls of Gymnophiona and their significance in the taxonomy of the group. The University of Kansas Science Bulletin, 48(15), 585–687.Google Scholar
  131. Teodecki, E. E., Brodie, E. D., Formanowicz, D. R., & Nussbaum, R. A. (1998). Head dimorphism and burrowing speed in the African caecilian Schistometopum thomense (Amphibia: Gymnophiona). Herpetologica, 54(2), 154–160.Google Scholar
  132. Trueb, L. (1993). Patterns of cranial diversity among the Lissamphibia. In J. Hanken & B. K. Hall (Eds.), The Skull: Patterns of Structural and Systematic Diversity (pp. 255–338). Chicago: The University of Chicago Press.Google Scholar
  133. Uyeda, J. C., Hansen, T. F., Arnold, S. J., & Pienaar, J. (2011). The million-year wait for macroevolutionary bursts. Proceedings of the National Academy of Sciences, 108(38), 15908–15913.Google Scholar
  134. Volume Graphics. 2001. VGStudio MAX version 2.0: Volume Graphics GmbH, Germany.Google Scholar
  135. Wake, M. H. (1993). The skull as a locomotor organ. In: J. Hanken & B. K. Hall (Eds.), The Skull: Functional and Evolutionary Mechanisms (pp. 197–240). Chicago: The University of Chicago Press.Google Scholar
  136. Wake, M. H. (2003). The osteology of caecilians. In: H. M. D. Heatwole (Ed.), Amphibian biology: Osteology (pp. 1809–1876) Chipping Norton: Surrey Beatty.Google Scholar
  137. Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., et al. (2007). Landmark Editor version 3.6: Institute for Data Analysis and Visualization, University of California, Davis.Google Scholar
  138. Wilkinson, M., Kupfer, A., Marques-Porto, R., Jeffkins, H., Antoniazzi, M., & Jared, C. (2008). One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona). Biology Letters, 4, 358–361.PubMedCentralPubMedGoogle Scholar
  139. Wilkinson, M., & Nussbaum, R. A. (1998). Caecilian viviparity and amniote origins. Journal of Natural History, 32(9), 1403–1409.Google Scholar
  140. Wilkinson, M., & Nussbaum, R. A. (1999). Evolutionary relationships of the lungless caecilian Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae). Zoological Journal of the Linnean Society, 126(2), 191–223.Google Scholar
  141. Wilkinson, M., & Nussbaum, R. A. (2006). Caecilian phylogeny and classification. In J. M. Exbrayat (Ed.), Reproductive biology and phylogeny of Gymnophiona (caecilians) (pp. 39–78). Enfield NH: Science Pubs Inc.Google Scholar
  142. Wilkinson, M., Presswell, B., Sherratt, E., Papadopoulou, A., & Gower, D. J. (2014). A new species of striped Ichthyophis Fitzinger, 1826 (Amphibia: Gymnophiona: Ichthyophiidae) from Myanmar. Zootaxa, 3785(1), 45–58.PubMedGoogle Scholar
  143. Wilkinson, M., San Mauro, D., Sherratt, E., & Gower, D. J. (2011). A nine-family classification of caecilians (Amphibia: Gymnophiona). Zootaxa, 2874, 41–64.Google Scholar
  144. Wilkinson, M., Sebben, A., Schwartz, E. N. F., & Schwartz, C. A. (1998). The largest lungless tetrapod: Report on a second specimen of Atretochoana eiselti (Amphibia: Gymnophiona: Typhlonectidae) from Brazil. Journal of Natural History, 32(4), 617–627.Google Scholar
  145. Wilkinson, M., Sherratt, E., Starace, F., & Gower, D. J. (2013). A new species of skin-feeding caecilian and the first report of reproductive mode in Microcaecilia (Amphibia: Gymnophiona: Siphonopidae). PLoS ONE, 8(3), e57756.PubMedCentralPubMedGoogle Scholar
  146. Wilkinson, M., Thorley, J. L., Littlewood, D. T. J., & Bray, R. A. (2001). Towards a phylogenetic supertree of Platyhelminthes. In R. A. Bray (Ed.), Littlewood DTJ. Taylor and Francis: Interrelationships of the Platyhelminthes.Google Scholar
  147. Wollenberg, K., & Measey, J. (2009). Why colour in subterranean vertebrates? Exploring the evolution of colour patterns in caecilian amphibians. Journal of Evolutionary Biology, 22(5), 1046–1056.Google Scholar
  148. Wroe, S., & Milne, N. (2007). Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evolution, 61(5), 1251–1260.PubMedGoogle Scholar
  149. Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: a primer (p. 478). Amsterdam: Elsevier.Google Scholar
  150. Zhang, P., & Wake, M. H. (2009). A mitogenomic perspective on the phylogeny and biogeography of living caecilians. Molecular Phylogenetics and Evolution, 53, 479–491.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Emma Sherratt
    • 1
    • 2
    • 3
  • David J. Gower
    • 1
  • Christian Peter Klingenberg
    • 2
  • Mark Wilkinson
    • 1
  1. 1.Department of Zoology (Currently the Department of Life Sciences)The Natural History MuseumLondonUK
  2. 2.Faculty of Life SciencesUniversity of ManchesterManchesterUK
  3. 3.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA

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