Ossification sequence of the common tern (Sterna hirundo) and its implications for the interrelationships of the Lari (Aves, Charadriiformes)

Journal of Morphology

Volumn 269, Issue 9, 2008, Pages 1056-1072

  Maxwell, Erin E ^a   Harrison, Luke B ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Aves; Charadriiformes; Ontogeny; Ossification sequence; Skeletal development

Indexed keywords

ANIMAL; ARTICLE; BONE DEVELOPMENT; CHARADRIIFORMES; CLASSIFICATION; EVOLUTION; FORELIMB; HINDLIMB; HISTOLOGY; PHYLOGENY; PHYSIOLOGY; SKULL;

ANIMALS; CHARADRIIFORMES; EVOLUTION; FORELIMB; HINDLIMB; OSTEOGENESIS; PHYLOGENY; SKULL;

AVES; CATHARACTA SKUA; CHARADRII; CHARADRIIFORMES; LARIDAE; STERCORARIIDAE; STERNA HIRUNDO;

EID: 51549104657     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10633     Document Type: Article

References (74)

1. Adriaens D, Verraes W. 1998. Ontogeny of the osteocranium in the African catfish, Clarias gariepinus Burchell (1822) (Siluriformes: Clariidae): Ossification sequence as a response to functional demands. J Morphol 235:183-237.
2. Andersson M. 1999. Phylogeny, behaviour, plumage evolution and neoteny in skuas Stercorariidae. J Avian Biol 30:205-215.
3. Arendt JD, Wilson DS. 2000. Population differences in the onset of cranial ossification in pumpkinseed (Lepomis gibbosus), a potential cost of rapid growth. Can J Fish Aquat Sci 57:351-356.
4. Badyaev AV, Martin TE. 2000. Individual variation in growth trajectories: Phenotypic and genetic correlations in ontogeny of the House Finch (Carpodacus mexicanus). J Evol Biol 13:290-301.
5. Baumel JJ, Witmer LM. 1993. Osteologia. In: Baumel JJ, King AS, Breazile JE, Evans HE, Vanden Berge JC, editors. Handbook of Avian Anatomy, 2nd ed. Cambridge: Nuttall Ornithological Club. pp 45-132.
6. Bininda-Emonds ORP, Jeffery JE, Richardson MK. 2003. Is sequence heterochrony an important evolutionary mechanism in mammals? J Mamm Evol 10:335-361.
7. Cane WP. 1993. The ontogeny of postcranial integration in the common tern, sterna hirundo. Evolution 47:1138-1151.
8. Cane WP. 1994. Ontogenetic evidence for relationships within the Laridae. Auk 111:873-880.
9. Christian PD, Christidis L, Schodde R. 1992. Biochemical systematics of the Charadriiformes (shorebirds): Relationships between the Charadrii, Scolopaci and Lari. Aust J Zool 40:291-302.
10. Chu PC. 1995. Phylogenetic reanalysis of Strauch's osteological data set for the Charadriiformes. Condor 97:174-196.
11. Chu PC. 1998. A phylogeny of the gulls (Aves: Larinae) inferred from osteological and integumentary characters. Cladistics 14:1-43.
12. Dingerkus G, Uhler LD. 1977. Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol 52:229-232.
13. Ericson PGP, Envall I, Irestedt M, Norman JA. 2003. Inter-familial relationships of the shorebirds (Aves: Charadriiformes) based on nuclear DNA sequence data. BMC Evol Biol 3:1-14.
14. Fain MG, Houde P. 2007. Multilocus perspectives on the monophyly and phylogeny of the order Charadriiformes (Aves). BMC Evol Biol 7:15.
15. Fröbisch NB. Ossification patterns in the tetrapod limb - Conservation and divergence from morphogenetic events. Biol Rev (in press).
16. Goldschmid A. 1972. Die Entwicklung des Craniums der Mausvögel (Coliidae, Coliiformes, Aves). IV. Die Entwicklung des Osteocraniums. Gegenbaurs Morphol Jahrb 118:553-569.
17. Goswami A. 2007. Cranial modularity and sequence heterochrony in mammals. Evol Dev 9:290-298.
18. Hall BK. 2001. Development of the clavicles in birds and mammals. J Exp Zool 289:153-161.
19. Haluska F, Alberch P. 1983. The cranial development of Elaphe obsoleta (Ophidia, Colubridae). J Morphol 178:37-55.
20. Harrison LB, Larsson HCE. Estimating evolution of temporal sequence changes: A practical approach to inferring ancestral developmental sequences and sequence heterochrony. Syst Biol (in press).
21. Jeffery JE, Bininda-Emonds ORP, Coates MI, Richardson MK. 2005. A new technique for identifying sequence heterochrony. Syst Biol 54:230-240.
22. Jollie MT. 1957. The head skeleton of the chicken and remarks on the anatomy of this region in other birds. J Morphol 100:389-436.
23. Leighton VL. 1894. The development of the wing of Sterna wilsonii. Am Nat 28:761-774.
24. Livezey BC. 1991. A phylogenetic analysis and classification of recent dabbling ducks (Tribe Anatini) based on comparative morphology. Auk 108:471-507.
25. Livezey BC. 1996. A phylogenetic reassessment of the Tadornine - Anatine divergence (Aves: Anseriformes; Anatidae). Ann Carnegie Mus 65:27-88.
26. Livezey BC. 1998. A phylogenetic analysis of the Gruiformes (Aves) based on morphological characters, with an emphasis on the Rails (Rallidae). Phil Trans R Soc London B Biol Sci 353:2077-2151.
27. Livezey BC, Zusi RL. 2001. Higher-order phylogenetics of modern Aves based on comparative anatomy. Netherlands J Zool 51:179-205.
28. Livezey BC, Zusi RL. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool J Linn Soc 149:1-95.
29. Mabee PM. 2000. The usefulness of ontogeny in interpreting morphological characters. In: Wiens JJ, editor. Phylogenetic Analysis of Morphological Data. Washington: Smithsonian Institution Press. pp 84-114.
30. Mabee PM, Olmstead KL, Cubbage CC. 2000. An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54:2091-2106.
31. Maillard J. 1948. Recherches embryologiques sur Catharacta skua Brünn (pterylose et ossification). Rev Suisse Zool 55:1-113.
32. Maisano JA. 2002a. Postnatal skeletal ontogeny in five xantusiids (Squamata: Scleroglossa). J Morphol 254:1-38.
33. Maisano JA. 2002b. The potential utility of postnatal skeletal developmental patterns in squamate phylogenetics. Zool J Linn Soc 136:277-313.
34. Maxwell EE. 2008. Comparative embryonic development of the skeleton of the domestic turkey (Meleagris gallopavo). Zoology 111:242-257.
35. Maxwell EE, Larsson HCE. 2007. Osteology and myology of the wing of the Emu (Dromaius novaehollandiae), and its bearing on the evolution of vestigial structures. J Morphol 268:423-441.
36. Mayr G, Clarke J. 2003. The deep divergences of neornithine birds: A phylogenetic analysis of morphological characters. Cladistics 19:527-553.
37. McGowan C. 1984. Evolutionary relationships of ratites and carinates: Evidence from ontogeny of the tarsus. Nature 307:733-735.
38. Mickevich MF, Parenti LR. 1980. Review of the phylogeny of the Charadriiformes (Aves): A new estimate using the method of character compatibility analysis. Syst Biol 29:108-113.
39. Minelli A. 2003. The Development of Animal Form: Ontogeny, Morphology and Evolution. New York: Cambridge University Press. 323 p.
40. Nakane Y, Tsudzuki M. 1999. Development of the skeleton in Japanese quail embryos. Dev Growth Differ 41:523-534.
41. Nisbet ICT. 2002. Common Tern (Sterna hirundo). In: Poole A, Gill F, editors. The Birds of North America. Philadelphia: The birds of North America Inc. p 618.
42. Paton TA, Baker AJ. 2006. Sequences from 14 mitochondrial genes provide a well-supported phylogeny of the charadriiform birds congruent with the nuclear RAG-1 tree. Mol Phylogenet Evol 39:657-667.
43. Paton TA, Baker AJ, Groth JG, Barrowclough GF. 2003. RAG-1 sequences resolve phylogenetic relationships within Charadriiform birds. Mol Phylogenet Evol 29:268-278.
44. Pierotti RJ, Good TP. 1994. Herring Gull (Larus argentatus). In: Poole A, Gill F, editors. The Birds of North America. Philadelphia: The Academy of Natural Sciences. p 1-28.
45. Poe S. 2004. A test for patterns of modularity in sequences of developmental events. Evolution 58:1852-1855.
46. Pontoppidan E. 1763. Den Danske atlas eller Konge-Riget Dannemark, med dets naturlige egenskaber, elementer, indbyggere, værter, dyr og andre affødninger, dets gamle tildragelser og nærværende omstændingheder i alle provintzer, stæder, kirker, slotte og herre-gaarde. Forestillet ved en udførlig lands-beskrivelse, saa og oplyst med dertil forfærdigede landkort over enhver provintz, samt ziret med stædernes prospecter, grund-ridser, og andre merkværdige kaabber-stykker. Efter Søy-kongelig allernaadigst befalning.. Kiøbenhavn: Godiche. 723 p.
47. Prochel J. 2006. Early skeletal development in Talpa europaea, the common European mole. Zool Sci 23:427-434.
48. Richman JM, Buchtová M, Boughner JC. 2006. Comparative ontogeny and phylogeny of the upper jaw skeleton in amniotes. Dev Dyn 235:1230-1243.
49. Rogulska T. 1962. Differences in the process of ossification during the embryonic development of the chick (Gallus domesticus L.), Rook (Corvus frugilegus L.) and Black-Headed Gull (Larus ridibundus L.). Zool Pol 12:223-236.
50. Romanoff AL. 1960. The Avian Embryo: Structural and Functional Development. New York: Macmillan Company. 1305 p.
51. Rotthowe K, Starck JM. 1998. Evidence for a phylogenetic position of button quails (Turnicidae: Aves) among the Gruiformes. J Zool Syst Evol Res 36:39-51.
52. Sánchez-Villagra MR. 2002. Comparative patterns of postcranial ontogeny in therian mammals: An analysis of relative timing of ossification events. J Exp Zool B Mol Dev 294:264-273.
53. Schinz R, Zangerl R. 1937. Beiträge zur Osteogenese des Knochensystems beim Haushuhn, bei der und beim Haubensteissfuss. Denkschriften der Schweizerischen Naturforschenden Gesellschaft Abteilung 2 72:116-162.
54. Schnell GD. 1970. A phenetic study of the suborder Lari (Aves) I. Methods and results of principal components analysis. Syst Zool 19:35-57.
55. Schulmeister S, Wheeler WC. 2004. Comparative and phylogenetic analysis of developmental sequences. Evol Dev 6: 50-57.
56. Schumacher GH, Wolff E. 1966a. Zur vergleichenden Osteogenese von Gallus domesticus L. Larus ridibundus L. und Larus canus L. I. Zeitliches Erscheinen der Ossifikationen bei Gallus domesticus L. Gegenbaurs Morphol Jahrb 110:359-373.
57. Schumacher GH, Wolff E. 1966b. Zur vergleichenden Osteogenese von Gallus domesticus L. Larus ridibundus L. und Larus canus L. II. Zeitliches Erscheinen der Ossifikationen bei Larus ridibundus L. und Larus canus L. Gegenbaurs Morphol Jahrb 110:620-635.
58. Sibley CG, Ahlquist JE. 1990. Phylogeny and Classification of Birds. New Haven: Yale University Press.
59. Smith KK. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51:1663-1678.
60. Smith KK. 2001. Heterochrony revisited: The evolution of developmental sequences. Biol J Linn Soc 73:169-186.
61. Starck JM. 1989. Zeitmuster der Ontogenesen bei nestflüchtenden und nesthockenden Vögeln. Stuttgart: E. Schweizerbartsche Verlagsbuchhandlung. 318 p.
62. Starck JM. 1993. Evolution of avian ontogenies. Curr Ornithol 10:275-366.
63. Starck JM. 1996. Comparative morphology and cytokinetics of skeletal growth in hatchlings of altricial and precocial birds. Zool Anz 235:53-75.
64. Starck JM. 1998. Structural variants and invariants in avian embryonic and postnatal development. In: Starck JM, Ricklefs RE, editors. Avian Growth and Development: Evolution Within the Altricial-Precocial Spectrum. New York: Oxford University Press. pp 59-88.
65. Starck JM, Ricklefs RE. 1998. Patterns of development: The altricial-precocial spectrum. In: Starck JM, Ricklefs RE, editors. Avian Growth and Development: Evolution Within the Altricial-Precocial Spectrum. New York: Oxford University Press. pp 3-30.
66. Starck JM, Sutter E. 2000. Patterns of growth and heterochrony in moundbuilders (Megapodiidae) and fowl (Phasianidae). J Avian Biol 31:527-547.
67. Strauch JGJ. 1978. The phylogeny of Charadriiformes (Aves): A new estimate using the method of character compatibility analysis. Trans Zool Soc London 34:263-345.
68. Strong RM. 1925. The order, time, and rate of ossification of the albino rat (Mus norvegicus albinus) skeleton. Am J Anat 36:313-355.
69. Swofford DL. 1998. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sunderland, Massachussetts: Sinauer Associates.
70. Thomas GH, Wills MA, Székely T. 2004. Phylogeny of shorebirds, gulls, and alcids (Aves: Charadrii) from the cytochrome-b gene: Parsimony, Bayesian inference, minimum evolution, and quartet puzzling. Mol Phylogenet Evol 30:516-526.
71. Velhagen WA Jr. 1997. Analyzing developmental sequences using sequence units. Syst Biol 46:204-210.
72. White CD. 1996. Suturai effects of fronto-occipital cranial modification. Am J Phys Anthropol 100:397-410.
73. Zusi RL. 1984. A functional and evolutionary analysis of rhynchokinesis in birds. Smithson Contrib Zool 395:1-40.
74. Zusi RL, Livezey BC. 2000. Homology and phylogenetic implications of some enigmatic cranial features in galliform and anseriform birds. Ann Carnegie Mus 69:157-193.