Evolutionary Biology

, Volume 42, Issue 4, pp 502–510 | Cite as

Altriciality and the Evolution of Toe Orientation in Birds

  • João Francisco Botelho
  • Daniel Smith-Paredes
  • Alexander O. Vargas
Synthesis Paper


Specialized morphologies of bird feet have evolved several times independently as different groups have become zygodactyl, semi-zygodactyl, heterodactyl, pamprodactyl or syndactyl. Birds have also convergently evolved similar modes of development, in a spectrum that goes from precocial to altricial. Using the new context provided by recent molecular phylogenies, we compared the evolution of foot morphology and modes of development among extant avian families. Variations in the arrangement of toes with respect to the anisodactyl ancestral condition have occurred only in altricial groups. Those groups represent four independent events of super-altriciality and many independent transformations of toe arrangements (at least four zygodactyl, three semi-zygodactyl, one heterodactyl, one pamprodactyl group, and several syndactyl). We propose that delayed skeletal maturation due to altriciality facilitates the epigenetic influence of embryonic muscular activity over developing toes, allowing for repeated evolution of innovations in their morphology.


Altricial Anisodactyl Heterodactyl Pamprodactyl Precocial Syndactyl Zygodactyl 



We are thankful to Macarena Faunes, Jorge Mpodozis, Sergio Soto-Acuña, Mauricio Cornejo, Vítor Piacentini and Gonzalo Marín for the useful commentaries on the manuscript. Daniel Nuñez-Leon kindly provided some bird photos.

Compliance with Ethical Standards


This Project was funded by FONDECYT (1150906).


  1. Alberch, P. (1982). Developmental constraints in evolutionary processes. In J. T. Bonner (Ed.), Evolution and Development (pp. 313–332). Berlin: Springer.CrossRefGoogle Scholar
  2. Arthur, W. (2001). Developmental drive: An important determinant of the direction of phenotypic evolution. Evolution and Development, 3(4), 271–278.CrossRefPubMedGoogle Scholar
  3. Baird, R. F., & Vickers-Rich, P. (1997). Eutreptodactylus itaboraiensisgen. et sp. nov., an early cuckoo (Aves: Cuculidae) from the Late Paleocene of Brazil. Alcheringa: An Australasian Journal of Palaeontology, 21(2), 123–127. doi: 10.1080/03115519708619179.CrossRefGoogle Scholar
  4. Balanoff, A. M., Bever, G. S., Rowe, T. B., & Norell, M. A. (2013). Evolutionary origins of the avian brain. Nature, 501(7465), 93–96. doi: 10.1038/nature12424.CrossRefPubMedGoogle Scholar
  5. Bell, A., & Chiappe, L. M. (2011). Statistical approach for inferring ecology of Mesozoic birds. Journal of Systematic Palaeontology, 9(1), 119–133.CrossRefGoogle Scholar
  6. Berger, A. J. (1960). Some anatomical characters of the Cuculidae and the Musophagidae. The Wilson Bulletin, 72(1), 60–104.Google Scholar
  7. Bhullar, B. A., Marugan-Lobon, J., Racimo, F., Bever, G. S., Rowe, T. B., Norell, M. A., et al. (2012). Birds have paedomorphic dinosaur skulls. Nature, 487(7406), 223–226. doi: 10.1038/nature11146.CrossRefPubMedGoogle Scholar
  8. Birchard, G. F., Ruta, M., & Deeming, D. C. (2013). Evolution of parental incubation behaviour in dinosaurs cannot be inferred from clutch mass in birds. Biology Letters, 9(4), 20130036. doi: 10.1098/rsbl.2013.0036. ISSN: 1744-957X.
  9. Bock, W. J., & Miller, W. D. (1959). The scansorial foot of the woodpeckers, with comments on the evolution of perching and climbing feet in birds. American Museum Novitates, 1931, 1–45.Google Scholar
  10. Botelho, J. F., Smith-Paredes, D., Nuñez-Leon, D., Soto-Acuña, S., & Vargas, A. O. (2014). The developmental origin of zygodactyl feet and its possible loss in the evolution of Passeriformes. Proceedings of the Royal Society B: Biological Sciences,. doi: 10.1098/rspb.2014.0765.PubMedCentralPubMedGoogle Scholar
  11. Botelho, J. F., Smith-Paredes, D., Soto-Acuña, S., Mpodozis, J., Palma, V., & Vargas, A. O. (2015). Skeletal plasticity in response to embryonic muscular activity underlies the development and evolution of the perching digit of birds. Scientific Reports,. doi: 10.1038/srep09840.Google Scholar
  12. Caponi, G. (2012). Réquiem por el Centauro: Aproximación epistemológica a la biología evolucionaria del desarrollo. México: Centro de Estudios Filosóficos y Sociales Vicente Lombardo Toledano.Google Scholar
  13. Clark, G. A. (1981). Toe fusion in oscines. The Wilson Bulletin, 93(1), 67–76.Google Scholar
  14. Collins, C. T. (1983). A reinterpretation of pamprodactyly in swifts: A convergent grasping mechanism in vertebrates. The Auk, 100(3), 735–737.Google Scholar
  15. Cracraft, J. (1971a). The functional morphology of the hind limb of the domestic pigeon, Columba livia. Bulletin of the AMNH. Bulletin of the American Museum of Natural History, 144, 172–267.Google Scholar
  16. Cracraft, J. (1971b). The relationships and evolution of the rollers: Families Coraciidae, Brachypteraciidae, and Leptosomatidae. The Auk, 88(4), 723–752.CrossRefGoogle Scholar
  17. Cuvier, G. (1836). Le règne animal distribué d’après son organisation, pour servir de base à l’histoire naturelle des animaux et d’introduction à l’anatomie comparée (Vol. 3). Paris: Louis Hauman et Comp., libraires-éditeurs.CrossRefGoogle Scholar
  18. Ericson, P. G., Anderson, C. L., Britton, T., Elzanowski, A., Johansson, U. S., Kallersjo, M., et al. (2006). Diversification of Neoaves: Integration of molecular sequence data and fossils. Biology Letters, 2(4), 543–547. doi: 10.1098/rsbl.2006.0523.PubMedCentralCrossRefPubMedGoogle Scholar
  19. Fain, M. G., & Houde, P. (2004). Parallel radiations in the primary clades of birds. Evolution, 58(11), 2558–2573.CrossRefPubMedGoogle Scholar
  20. Forbes, W. A. (1880). On the anatomy of Leptosoma discolor. Proceedings of the Zoological Society of London, 48(3), 465–475. doi: 10.1111/j.1469-7998.1880.tb06585.x.CrossRefGoogle Scholar
  21. Forbes-Watson, A. D. (1967). Observations at a nest of the cuckoo-roller Leptosomus discolor. Ibis, 109(3), 425–430. doi: 10.1111/j.1474-919X.1967.tb04015.x.CrossRefGoogle Scholar
  22. George, J. C., & Berger, A. J. (1966). Avian myology. New York: Academic Press.Google Scholar
  23. Goodman, S. (2001). Family leptosomatidae (Cuckoo-roller). In J. Hoyo, A. Elliot, & J. Sargatal (Eds.), Handbook of the birds of the world. Mousebirds to hornbills (Vol. 6, pp. 390–395). Barcelona: Lynx Edicions.Google Scholar
  24. Grady, J. M., Enquist, B. J., Dettweiler-Robinson, E., Wright, N. A., & Smith, F. A. (2014). Evidence for mesothermy in dinosaurs. Science, 344(6189), 1268–1272.CrossRefPubMedGoogle Scholar
  25. Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C., Braun, E. L., Braun, M. J., et al. (2008). A phylogenomic study of birds reveals their evolutionary history. Science, 320(5884), 1763–1768. doi: 10.1126/science.1157704.CrossRefPubMedGoogle Scholar
  26. Hall, B. K., & Herring, S. W. (1990). Paralysis and growth of the musculoskeletal system in the embryonic chick. Journal of Morphology, 206(1), 45–56. doi: 10.1002/jmor.1052060105.CrossRefPubMedGoogle Scholar
  27. Hudson, G. E. (1937). Studies on the muscles of the pelvic appendage in birds. American Midland Naturalist, 18(1), 1–108.CrossRefGoogle Scholar
  28. Hudson, G. E. (1948). Studies on the muscles of the pelvic appendage in birds II: The heterogeneous order falconiformes. American Midland Naturalist, 39(1), 102–127.CrossRefGoogle Scholar
  29. Jarvis, E. D., Mirarab, S., Aberer, A. J., Li, B., Houde, P., Li, C., et al. (2014). Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346(6215), 1320–1331.PubMedCentralCrossRefPubMedGoogle Scholar
  30. Kimball, R. T., Wang, N., Heimer-McGinn, V., Ferguson, C., & Braun, E. L. (2013). Identifying localized biases in large datasets: A case study using the avian tree of life. Molecular Phylogenetics and Evolution, 69(3), 1021–1032. doi: 10.1016/j.ympev.2013.05.029.CrossRefPubMedGoogle Scholar
  31. Ksepka, D. T., & Clarke, J. A. (2012). A new stem parrot from the Green River Formation and the complex evolution of the grasping foot in Pan-Psittaciformes. Journal of Vertebrate Paleontology, 32(2), 395–406. doi: 10.1080/02724634.2012.641704.CrossRefGoogle Scholar
  32. Laland, K. N., Sterelny, K., Odling-Smee, J., Hoppitt, W., & Uller, T. (2011). Cause and effect in biology revisited: Is Mayr’s proximate-ultimate dichotomy still useful? Science, 334(6062), 1512–1516.CrossRefPubMedGoogle Scholar
  33. Livezey, B. C., & Zusi, R. L. (2007). Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnean Society, 149(1), 1–95. doi: 10.1111/j.1096-3642.2006.00293.x.PubMedCentralCrossRefPubMedGoogle Scholar
  34. Maurer, D. R., & Raikow, R. J. (1981). Appendicular myology, phylogeny, and classification of the avian order Coraciiformes (including Trogoniformes). Annals of the Carnegie Museum, 50(18), 417–434.Google Scholar
  35. Mayr, E. (1961). Cause and effect in biology. Science, 134, 1501–1506.CrossRefPubMedGoogle Scholar
  36. Mayr, G. (2003). On the phylogenetic relationships of trogons (Aves, Trogonidae). Journal of Avian Biology, 34(1), 81–88. doi: 10.1034/j.1600-048X.2003.03042.x.CrossRefGoogle Scholar
  37. Mayr, G. (2005). A Fluvioviridavis-like bird from the Middle Eocene of Messel, Germany. Canadian Journal of Earth Sciences, 42(11), 2021–2037.CrossRefGoogle Scholar
  38. Mayr, G. (2006). A specimen of Eocuculus Chandler, 1999 (Aves,? Cuculidae) from the early Oligocene of France. Geobios, 39(6), 865–872. doi: 10.1016/j.geobios.2005.10.007.CrossRefGoogle Scholar
  39. Mayr, G. (2008a). The Madagascan “cuckoo-roller” (Aves: Leptosomidae) is not a roller—Notes on the phylogenetic affinities and evolutionary history of a “living fossil”. Acta Ornithologica, 43(2), 226–230. doi: 10.3161/000164508x395360.CrossRefGoogle Scholar
  40. Mayr, G. (2008b). Phylogenetic affinities of the enigmatic avian taxon Zygodactylus based on new material from the early oligocene of France. Journal of Systematic Palaeontology, 6(3), 333–344. doi: 10.1017/s1477201907002398.CrossRefGoogle Scholar
  41. Mayr, G. (2009). Paleogene fossil birds. Berlin: Springer.CrossRefGoogle Scholar
  42. Mayr, G. (2010). Phylogenetic relationships of the paraphyletic ‘caprimulgiform’ birds (nightjars and allies). Journal of Zoological Systematics and Evolutionary Research, 48(2), 126–137. doi: 10.1111/j.1439-0469.2009.00552.x.CrossRefGoogle Scholar
  43. Mayr, G. (2011). Well-preserved new skeleton of the Middle Eocene Messelastur substantiates sister group relationship between Messelasturidae and Halcyornithidae (Aves,? Pan-Psittaciformes). Journal of Systematic Palaeontology, 9(1), 159–171. doi: 10.1080/14772019.2010.505252.CrossRefGoogle Scholar
  44. Mayr, G., Rana, R. S., Rose, K. D., Sahni, A., Kumar, K., Singh, L., et al. (2010). Quercypsitta-like birds from the early Eocene of India (Aves,? Psittaciformes). Journal of Vertebrate Paleontology, 30(2), 467–478. doi: 10.1080/02724631003617357.CrossRefGoogle Scholar
  45. Mayr, G., Rana, R., Rose, K., Sahni, A., Kumar, K., & Smith, T. (2013). New specimens of the early Eocene bird Vastanavis and the interrelationships of stem group Psittaciformes. Paleontological Journal, 47(11), 1308–1314. doi: 10.1134/S0031030113110105.CrossRefGoogle Scholar
  46. McCormack, J. E., Harvey, M. G., Faircloth, B. C., Crawford, N. G., Glenn, T. C., & Brumfield, R. T. (2013). A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS One, 8(1), e54848. doi: 10.1371/journal.pone.0054848.PubMedCentralCrossRefPubMedGoogle Scholar
  47. Mitchell, J. S., & Makovicky, P. J. (2014). Low ecological disparity in early Cretaceous birds. Proceedings of the Royal Society B: Biological Sciences, 281(1787), 20140608.PubMedCentralCrossRefPubMedGoogle Scholar
  48. Mourer-Chauviré, C., Tabuce, R., Essid, E. M., Marivaux, L., Khayati, H., Vianey-Liaud, M., et al. (2013). A new taxon of stem group Galliformes and the earliest record for stem group Cuculidae from the Eocene of Djebel Chambi, Tunisia. In U. B. Göhlich & A. Kroh (Eds.), Proceedings of the 8th International Meeting of the Society of Avian Paleontology and Evolution. Austria: Verlag Naturhistorisches Museum Wien.Google Scholar
  49. Muller, G. B. (2003). Embryonic motility: Environmental influences and evolutionary innovation. Evolution and Development, 5(1), 56–60.CrossRefPubMedGoogle Scholar
  50. Murray, P. D. F., & Drachman, D. B. (1969). The role of movement in the development of joints and related structures: The head and neck in the chick embryo. Journal of Embryology and Experimental Morphology, 22(3), 349–371.PubMedGoogle Scholar
  51. Nesbitt, S. J., Ksepka, D. T., & Clarke, J. A. (2011). Podargiform affinities of the enigmatic Fluvioviridavis platyrhamphus and the early diversification of Strisores (“Caprimulgiformes” + Apodiformes). PLoS One, 6(11), e26350. doi: 10.1371/journal.pone.0026350.PubMedCentralCrossRefPubMedGoogle Scholar
  52. Newman, S. A., Mezentseva, N. V., & Badyaev, A. V. (2013). Gene loss, thermogenesis, and the origin of birds. Annals of the New York Academy of Sciences, 1289(1), 36–47.CrossRefPubMedGoogle Scholar
  53. Newman, S. A., & Muller, G. B. (2005). Origination and innovation in the vertebrate limb skeleton: An epigenetic perspective. Journal of Experimental Zoology Part B Molecular and Developmental Evolution, 304(6), 593–609. doi: 10.1002/jez.b.21066.CrossRefGoogle Scholar
  54. Nice, M. M. (1962). Development of behavior in precocial birds. Transactions of the Linnean Society, 8, 1–212.Google Scholar
  55. Pitsillides, A. (2006). Early effects of embryonic movement: “A shot out of the dark”. Journal of Anatomy, 208(4), 417.PubMedCentralCrossRefPubMedGoogle Scholar
  56. Raikow, R. J. (1985). Locomotor system. In A. S. King & J. McLelland (Eds.), Form and function in birds (Vol. 3, pp. 57–147). London: Academic Press.Google Scholar
  57. Raikow, R. J. (1987). Hindlimb Myology and evolution of the old world suboscine passerine birds (Acanthisittidae, Pittidae, Philepittidae, Eurylaimidae). Ornithological Monographs, 41, 7–81.Google Scholar
  58. Ray, A., Singh, P. N. P., Sohaskey, M. L., Harland, R. M., & Bandyopadhyay, A. (2015). Precise spatial restriction of BMP signaling is essential for articular cartilage differentiation. Development, 142(6), 1169–1179.CrossRefPubMedGoogle Scholar
  59. Ricklefs, R. E. (1984). The optimization of growth rate in altricial birds. Ecology, 65(5), 1602–1616. doi: 10.2307/1939139.CrossRefGoogle Scholar
  60. Starck, J. M. (1993). The evolution of avian ontogeny. In D. M. Power (Ed.), Current Ornithology (Vol. 10, pp. 275–366). New York: Plenum Press.CrossRefGoogle Scholar
  61. Starck, J. M. (1998). Structural variants and invariants in avian embryonic and postnatal development. In J. M. Starck & R. E. Ricklefs (Eds.), Avian growth and development: Evolution within the altricial-precocial spectrum (pp. 59–88). New York: Oxford University Press.Google Scholar
  62. Starck, J. M., & Ricklefs, R. E. (1998). Patterns of development: The altricial-precocial spectrum. In J. M. Starck & R. E. Ricklefs (Eds.), Avian growth and development (Oxford ornithology series) (Vol. 8, pp. 3–30). New York: Oxford University Press.Google Scholar
  63. Swierczewski, E. V., & Raikow, R. J. (1981). Hind limb morphology, phylogeny, and classification of the piciformes. The Auk, 98, 466–480.Google Scholar
  64. Tullberg, B. S., Ah-King, M., & Temrin, H. (2002). Phylogenetic reconstruction of parental-care systems in the ancestors of birds. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 357(1419), 251–257. doi: 10.1098/rstb.2001.0932.PubMedCentralCrossRefPubMedGoogle Scholar
  65. Wetmore, A. (1934). A systematic classification for the birds of the world, revised and amended. Smithsonian Miscellaneous Collections, 89(13), 1–11.Google Scholar
  66. Winslow, B. B., & Burke, A. C. (2010). Atypical molecular profile for joint development in the avian costal joint. Developmental Dynamics, 239(10), 2547–2557. doi: 10.1002/dvdy.22388.PubMedCentralCrossRefPubMedGoogle Scholar
  67. Yuri, T., Kimball, R. T., Harshman, J., Bowie, R. C., Braun, M. J., Chojnowski, J. L., et al. (2013). Parsimony and model-based analyses of indels in avian nuclear genes reveal congruent and incongruent phylogenetic signals. Biology, 2(1), 419–444. doi: 10.3390/biology2010419.PubMedCentralCrossRefPubMedGoogle Scholar
  68. Zelenkov, N. V. (2007). The structure and probable mechanism of evolutionary formation of the foot in piciform birds (Aves: Piciformes). Paleontological Journal, 41(3), 290–297. doi: 10.1134/s0031030107030082.CrossRefGoogle Scholar
  69. Zusi, R. L., & Bentz, G. D. (1984). Myology of the purple-throated carib (Eulampis jugularis) and other hummingbirds (Aves: Trochilidae). Smithsonian Contributions to Zoology, 385, 1–70. doi: 10.5479/si.00810282.385.Google Scholar

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© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Laboratorio de Ontogenia y Filogenia, Departamento de BiologíaFacultad de Ciencias de la Universidad de ChileSantiagoChile

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