Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-27T15:44:28.193Z Has data issue: false hasContentIssue false
  • English
  • Français

Patterns in the evolution of nares size and secondary palate length in anomodont therapsids (Synapsida): implications for hypoxia as a cause of end-Permian tetrapod extinctions

Published online by Cambridge University Press:  20 May 2016

Kenneth D. Angielczyk  and
Melony L. Walsh
Kenneth D. Angielczyk
Affiliation:
1Department of Geology, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605,
Melony L. Walsh
Affiliation:
2Department of Invertebrate Zoology & Geology, California Academy of Sciences, 875 Howard Street, San Francisco, California 94103
Get access Rights & Permissions [Opens in a new window]

Abstract

Seemingly consistent proportional differences in several palatal structures have been noted between Permian and Triassic anomodont therapsids for nearly a century. These patterns have been cited as evidence in support of a decline in atmospheric oxygen concentrations that may have contributed to end-Permian terrestrial extinctions. However, it is not known whether the observed differences are significant, or whether they stem from continued directional selection. If they are not significant, or if their timing does not match that proposed for the oxygen decline, support for the hypoxia-based extinction scenario would be weakened. We tested whether the internal nares and bony secondary palate, two palatal features proposed to be related to respiratory efficiency, are significantly larger in Triassic anomodonts, and whether the variation can be attributed to a long-term tendency for increase. Results based on raw data indicate that Triassic anomodonts have significantly larger secondary palates than Permian anomodonts. They also have significantly larger internal nares, but only when primitive, morphologically-divergent specimens are not considered. Although nares and palate size are correlated with stratigraphic occurrence, available data reject the hypothesis that the observed differences were the result of a long-term trend. Most of these findings are consistent with the predictions of the hypoxia scenario. However, removing the effects of body size and phylogeny causes some of the differences to break down, indicating that if selection for increased respiratory efficiency affected these characters, it was most likely not the only factor to do so. Therefore, the characters provide only weak evidence in support of the hypoxia scenario, and we recommend against their use for this purpose. Our results emphasize the need for caution when invoking presumed differences between Permian and Triassic vertebrates as support for hypoxia, or other extinction scenarios, without a rigorous study of the character(s) in question.

Type
Research Article
Information
Journal of Paleontology , Volume 82 , Issue 3 , May 2008 , pp. 528 - 542
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Angielczyk, K. D. 2001. Preliminary phylogenetic analysis and stratigraphic congruence of the dicynodont anomodonts (Synapsida: Therapsida). Palaeontologia Africana, 37:53–79.Google Scholar
Angielczyk, K. D. 2002. Redescription, phylogenetic position, and stratigraphic significance of the dicynodont genus Odontocyclops (Synapsida; Therapsida). Journal of Paleontology, 76:1047–1059.Google Scholar
Angielczyk, K. D. 2004. Phylogenetic evidence for and implications of a dual origin of propaliny in anomodont therapsids (Synapsida). Paleobiology, 30:268–296.Google Scholar
Angielczyk, K. D. 2007. New specimens of the Tanzanian dicynodont “Cryptocynodon” parringtoni Von Huene, 1942 (Therapsida, Anomodontia), with an expanded analysis of Permian dicynodont phylogeny. Journal of Vertebrate Paleontology, 27:116–131.Google Scholar
Angielczyk, K. D. and Kurkin, A. A. 2003. Phylogenetic analysis of Russian Permian dicynodonts (Therapsida: Anomodontia): Implications for Permian biostratigraphy and Pangaean biogeography. Zoological Journal of the Linnean Society, 139:157–212.Google Scholar
Beall, C. M. 1982. A comparison of chest morphology in high altitude Asian and Andean populations. Human Biology, 54:145–163.Google Scholar
Beall, C. M. 2000. Tibetan and Andean patterns of adaptation to high-altitude hypoxia. Human Biology, 72:201–228.Google Scholar
Beall, C. M. 2006. Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Integrative and Comparative Biology, 46:18–24.Google Scholar
Beall, C. M., Decker, M. J., Brittenham, G. M., Kushner, I., Gebremedhin, A., and Strohl, K. P. 2002. An Ethiopian pattern of human adaptation to high-altitude hypoxia. Proceedings of the National Academy of Sciences, 99:17215–17218.CrossRefGoogle ScholarPubMed
Beall, C. M., Strohl, K. P., Blangero, J., Williams-Blangero, S., Almasy, L. A., Decker, M. J., Worthman, C. M., Goldstein, M. C., Vargas, E., Villena, M., Soria, R., Alarcon, A. M., and Gonzales, C. 1997. Ventilation and hypoxic ventilatory response of Tibetan and Aymara high altitude natives. American Journal of Physical Anthropology, 104:427–447.Google Scholar
Bergman, N. M., Lenton, T. M., and Watson, A. J. 2004. COPSE: A new model of biogeochemical cycling over Phanerozoic time. American Journal of Science, 340:397–437.Google Scholar
Berner, R. A. 1987. Models for carbon and sulfur cycles and atmospheric oxygen: Application to Paleozoic geologic history. American Journal of Science, 287:177–196.Google Scholar
Berner, R. A. 1989. Drying, O2 and extinction. Nature, 340:603–604.Google Scholar
Berner, R. A. 1999. Atmospheric oxygen over Phanerozoic time. Proceedings of the National Academy of Science, 96:10955–10957.Google Scholar
Berner, R. A. 2001. Modeling atmospheric O2 over Phanerozoic time. Geochimica et Cosmochimica Acta, 65:685–694.Google Scholar
Berner, R. A. 2004. The Phanerozoic Carbon Cycle: CO2 and O2. Oxford University Press, Oxford, 158 p.Google Scholar
Berner, R. A. 2005. The carbon and sulfur cycles and atmospheric oxygen from middle Permian to middle Triassic. Geochimica et Cosmochimica Acta, 69:3211–17.Google Scholar
Berner, R. A. and Canfield, D. 1989. A new model for atmospheric oxygen over Phanerozoic time. American Journal of Science, 289:333–361.Google Scholar
Berner, R. A., Beerling, D. J., Dudley, R., Robinson, J. M., and Wildman, R. A. 2003. Phanerozoic atmospheric oxygen. Annual Reviews of Earth and Planetary Science, 31:105–134.Google Scholar
Botha, J. 2003. Biological aspects of the Permian dicynodont Oudenodon (Therapsida: Dicynodontia) deduced from bone histology and cross-sectional geometry. Palaeontologia Africana, 39:37–44.Google Scholar
Botha, J. and Angielczyk, K. D. 2007. An integrative approach to distinguishing the Late Permian dicynodont species Oudenodon bainii and Tropidostoma microtrema (Therapsida: Anomodontia). Palaeontology, 50: 1175–1209.Google Scholar
Botha, J. and Smith, R. M. H. 2006. Rapid vertebrate recuperation in the Karoo Basin of South Africa following the end-Permian extinction. Journal of African Earth Sciences, 45:502–514.CrossRefGoogle Scholar
Botha, J. and Smith, R. M. H. 2007. Lystrosaurus species composition across the Permo-Triassic boundary in the Karoo Basin of South Africa. Lethaia, 40:125–137.Google Scholar
Brooks, D. R. and McLennan, D. A. 1991. Phylogeny, Ecology, and Behavior. University of Chicago Press, Chicago, 434 p.Google Scholar
Brink, A. S. 1955. A study on the skeleton of Diademodon. Palaeontologia Africana, 3:3–39.Google Scholar
Camp, C. L. 1956. Triassic dicynodont reptiles, Pt. II, Triassic dicynodonts compared. Memoirs of the University of California, 13:305–341.Google Scholar
Cluver, M. A. and King, G. M. 1983. A reassessment of the relationships of Permian Dicynodontia (Reptilia, Therapsida) and a new classification of dicynodonts. Annals of the South African Museum, 91:195–273.Google Scholar
Cox, C. B. 1965. New Triassic dicynodonts from South America, their origins and relationships. Philosophical Transactions of the Royal Society of London Series B, 248:457–516.Google Scholar
Cox, C. B. 1998. The jaw function and adaptive radiation of the dicynodont mammal-like reptiles of the Karoo basin of South Africa. Zoological Journal of the Linnean Society, 122:349–384.Google Scholar
Cox, C. B. and Li, J.-L. 1983. A new genus of Triassic dicynodont from east Africa and its classification. Palaeontology, 26:389–406.Google Scholar
Cruickshank, A. R. I. 1962. East African Triassic Dicynodonts. Unpublished Ph.D. dissertation, University of Cambridge.Google Scholar
Cruickshank, A. R. I. 1967. A new dicynodont genus from the Manda Formation of Tanzania (Tanganyika). Journal of Zoology, 153:163–208.Google Scholar
Cruickshank, A. R. I. 1968. A comparison of the palates of Permian and Triassic dicynodonts. Palaeontologia Africana, 11:23–31.Google Scholar
Faraci, F. M. 1991. Adaptations to hypoxia in birds: How to fly high. Annual Review of Physiology, 53:59–70.Google Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist, 125:1–15.Google Scholar
Fröbisch, J. 2006. Locomotion in derived dicynodonts (Synapsida, Anomodontia): A functional analysis of the pelvic girdle and hind limb of Tetragonias njalilus. Canadian Journal of Earth Sciences, 43:1297–1308.Google Scholar
Fröbisch, J. 2007. The cranial anatomy of Kombuisia frerensis Hotton (Synapsida, Dicynodontia) and a new phylogeny of anomodont therapsids. Zoological Journal of the Linnean Society, 150:117–144.Google Scholar
Garland, T. and Ives, A. R. 2000. Using the past to predict the present: Confidence intervals for regression equations in phylogenetic comparative methods. American Naturalist, 155:346–364.Google Scholar
Garland, T., Bennett, A. F., and Rezende, E. L. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology, 208: 3015–3035.Google Scholar
Germain, D. and Laurin, M. 2005. Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zoologica Scripta, 34:335–350.CrossRefGoogle Scholar
Gittleman, J. L. and Luh, H.-K. 1992. On comparing comparative methods. Annual Review of Ecology and Systematics, 23:383–404.Google Scholar
Golubev, V. K. 2005. Permian Tetrapod Stratigraphy, p. 95–99. In Lucas, S. G. and Zeigler, K. E. (eds.), The Nonmarine Permian. New Mexico Museum of Natural History and Science Bulletin 30.Google Scholar
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of London Series B, 326:157–199.Google Scholar
Graham, J. B., Aguilar, N., Dudley, R., and Gans, C. 1995. The late Paleozoic atmosphere and the ecological and evolutionary physiology of tetrapods, p. 141–167. In Sumida, S. S. and Martin, K. L. (eds.), Amniote Origins. Academic Press, San Diego.Google Scholar
Graham, J. B., Dudley, R., Aguilar, N. M., and Gans, C. 1995. Implications of the late Paleozoic oxygen pulse for physiology and evolution. Nature, 375:117–120.Google Scholar
Grine, F. E., Foster, C. A., Cluver, M. A., and George, J. A. 2006. Cranial variability, ontogeny, and taxonomy of Lystrosaurus from the Karoo Basin of South Africa, p. 432–503. In Carrano, M. T., Gaudin, T. J., Blob, R. W., and Wible, J. R. (eds.), Amniote Paleobiology. University of Chicago Press, Chicago.Google Scholar
Hammond, K. A., Szewczak, J., and Krol, E. 2001. Effects of altitude and temperature on organ phenotypes plasticity along an altitudinal gradient. Journal of Experimental Biology, 204:1991–2000.Google Scholar
Harvey, P. H. and Pagel, M. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, 248 p.Google Scholar
Huey, R. B. and Ward, P. D. 2005. Hypoxia, global warming, and terrestrial Late Permian extinctions. Science, 308:398–401.CrossRefGoogle ScholarPubMed
Ivakhnenko, M. F., Golubev, V. K., Gubin, Y. M., Kalandadze, N. N., Novikov, I. V., Sennikov, A. G., and Rautian, A. S. 1997. Permian and Triassic Tetrapods of Eastern Europe. Geos, Moscow, 216 p.Google Scholar
Keyser, A. W. 1974. Evolutionary trends in Triassic Dicynodontia. Palaeontologia Africana, 17:57–68.Google Scholar
Keyser, A. W. 1979. A new dicynodont genus and its bearing on the origin of the Gondwana Triassic Dicynodontia, p. 184–198. In Laskar, B. and Raja Rao, C. S. (eds.), Proceedings and Papers of the 4th IUGS Gondwana Symposium. Hindustan Publishing Corporation, Delhi.Google Scholar
Keyser, A. W. and Cruickshank, A. R. I. 1979. The origins and classification of Triassic Dicynodonts. Transactions of the Geological Society of South Africa, 82:81–108.Google Scholar
King, G. M. 1988. Anomodontia. In Wellnhofer, P. (ed.), Handbuch der Paläoherpetologie. Volume 17c. Fischer Verlag, Stuttgart, 174 p.Google Scholar
King, G. M. 1994. The early anomodont Venjukovia and the evolution of the anomodont skull. Zoological Journal of the Linnean Society, 232:651–673.Google Scholar
Kitching, J. W. 1977. The distribution of the Karroo vertebrate fauna. Memoirs of the Bernard Price Institute for Palaeontological Research, 1:1–111.Google Scholar
Lasaga, A. C. 1989. A new approach to isotopic modeling of the variation of atmospheric oxygen through the Phanerozoic. American Journal of Science, 289:411–435.Google Scholar
Laurin, M. 2004. The evolution of body size, Cope's Rule and the origin of amniotes. Systematic Biology, 53:594–622.Google Scholar
Lorino, A. M., d'Ortho, M. P., Dahan, E., Bignani, O., Vastel, C., and Lorino, H. 2001. Combined effects of a nasal dilator and nasal prongs on nasal airflow resistance. Chest, 120:397–401.Google Scholar
Lorino, A. M., Lofaso, F., Drogou, I., Abi-Nader, F., Dahan, E., Coste, A., and Lorino, H. 1998. Effects of different mechanical treatments on nasal resistance assessed by rhinometry. Chest, 114:166–170.Google Scholar
Lucas, S. G. 1998. Global Trissic tetrapod biostratigraphy and biochronology. Palaeogeography, Palaeoclimatology, Palaeoecology, 143:347–384.Google Scholar
Lucas, S. G. 2002. Tetrapods and the subdivision of Permian time. Canadian Society of Petroleum Geologists Memoir, 19:479–491.Google Scholar
MacLeod, N. 2001. The role of phylogeny in quantitative paleobiological data analysis. Paleobiology, 27:226–240.Google Scholar
Maddison, W. P. 1991. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Systematic Zoology, 40:304–314.Google Scholar
Maddison, W. P. and Maddison, D. R. 2002. Mesquite: A modular system for evolutionary analysis. Version 1.05. http://mesquiteproject.org.Google Scholar
Maisch, M. W. 2001. Observations on Karoo and Gondwana vertebrates, Pt. 2, a new skull-reconstruction of Stahleckeria potens von Huene, 1935 (Dicynodontia, Middle Triassic) and a reconsideration of kannemeyeriiform phylogeny. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen, 220:127–152.Google Scholar
Maisch, M. W. 2002. A new basal lystrosaurid dicynodont from the Upper Permian of South Africa. Palaeontology, 45:343–359.Google Scholar
Maisch, M. W. and Gebauer, E. V. I. 2005. Reappraisal of Geikia locusticeps (Therapsida: Dicynodontia) from the Upper Permian of Tanzania. Palaeontology, 48:309–324.Google Scholar
Martins, E. P. 2005. COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. http://compare.bio.indiana.edu/.Google Scholar
Martins, E. P. and Hansen, T. F. 1997. Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist, 149:646–667.Google Scholar
Martins, E. P., Diniz-Filho, J. A. F., and Housworth, E. A. 2002. Adaptive constraints and the phylogenetic comparative method. Evolution, 56:1–13.Google ScholarPubMed
McAlester, A. L. 1970. Animal extinctions, oxygen consumption, and atmospheric history. Journal of Paleontology, 44:405–409.Google Scholar
McNab, B. K. 1978. The evolution of endothermy in the phylogeny of mammals. American Naturalist, 112:1–21.Google Scholar
Meissner, H.-H., Santiago, S. M., Koyal, S. N., Riemer, A., Sein, M., Goldman, M. D., and Williams, A. J. 1999. Characteristics of nasal airflow and the effect of a nasal dilator in normal human subjects. Respiration Physiology, 115:95–101.Google Scholar
Miles, D. B. and Dunham, A. E. 1993. Historical perspectives in ecology and evolutionary biology: The use of phylogenetic comparative analyses. Annual Review of Ecology and Systematics, 24:587–619.Google Scholar
Modesto, S. P. and Rybczynski, N. 2000. The amniote faunas of the Russian Permian: Implications for Late Permian terrestrial vertebrate biogeography, p. 17–34. In Benton, M. J., Shishkin, M. A., Unwin, D. M., and Kurochkin, E. N. (eds.), The Age of Dinosaurs in Russia and Mongolia. Cambridge University Press, Cambridge.Google Scholar
Modesto, S. P., Rubidge, B., and Welman, J. 1999. The most basal anomodont therapsid and the primacy of Gondwana in the evolution of the anomodonts. Proceedings of the Royal Society of London Series B, 266: 331–337.Google Scholar
Modesto, S. P., Rubidge, B., and Welman, J. 2002. A new dicynodont therapsid from the lowermost Beaufort Group, Upper Permian of South Africa. Canadian Journal of Earth Sciences, 39:1755–1765.Google Scholar
Modesto, S. P., Rubdige, B., Visser, I., and Welman, J. 2003. A new basal dicynodont from the Upper Permian of South Africa. Palaeontology, 46: 211–223.Google Scholar
Monge, C. and León-Velarde, F. 1991. Physiological adaptation to high altitude: Oxygen transport in mammals and birds. Physiological Reviews, 71:1135–1172.Google Scholar
Palomino, H., Mueller, W. H., and Schull, W. J. 1979. Altitude, heredity, and body proportions in northern Chile. American Journal of Physical Anthropology, 50:39–50.Google Scholar
Parrington, F. R. 1967. The origins of mammals. The Advancement of Science, 24:165–173.Google Scholar
Pearson, H. S. 1924. The skull of the dicynodont reptile Kannemeyeria. Proceedings of the Zoological Society London, 1924:793–826.Google Scholar
Ray, S. 2005. Lystrosaurus (Therapsida, Dicynodontia) from India: Taxonomy, relative growth, and cranial dimorphism. Journal of Systematic Palaeontology, 3:203–221.Google Scholar
Ray, S. 2006. Functional and evolutionary aspects of the postcranial anatomy of dicynodonts (Synapsida, Therapsida). Palaeontology, 49:1263–1286.Google Scholar
Ray, S. and Chinsamy, A. 2003. Functional aspects of the postcranial anatomy of the Permian dicynodont Diictodon and their ecological implications. Palaeontology, 46:151–183.Google Scholar
Ray, S., Chinsamy, A., and Bandyopadhyay, S. 2005. Lystrosaurus murrayi (Therapsida, Dicynodontia): Bone histology, growth, and lifestyle adaptations. Palaeontology, 48:1169–1185.Google Scholar
Renaut, A. J. 2001. Dicynodont jaw mechanisms reconsidered: The Kannemeyeria (Anomodontia Therapsida) masticatory cycle. Asociacion Paleontologica Argentina Publicacion Especial, 7:167–170.Google Scholar
Retallack, G. J. 2004. Vertebrate extinction across Permian-Triassic boundary in Karoo Basin, South Africa: Reply. Geological Society of America Bulletin, 116:1295–1296.Google Scholar
Retallack, G. J., Metzger, C. A., Greaver, T., Jahren, A. H., Smith, R. M. H., and Sheldon, N. D. 2006. Middle-Late Permian mass extinction on land. Geological Society of America Bulletin, 118:1398–1411.Google Scholar
Retallack, G. J., Smith, R. M. H., and Ward, P. D. 2003. Vertebrate extinction across Permian-Triassic boundary in Karoo Basin, South Africa. Geological Society of America Bulletin, 115:1133–1152.Google Scholar
Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55:2143–2160.Google Scholar
Rubidge, B. S. (Ed.). 1995. Biostratigraphy of the Beaufort Group (Karoo Supergroup). South African Committee for Stratigraphy Biostratigraphic Series, 1:1–46.Google Scholar
Rubidge, B. S. 2005. Re-uniting lost continents—fossil reptiles from the ancient Karoo and their wanderlust. South African Journal of Geology, 108: 135–172.Google Scholar
Rybczynski, N. 2000. Cranial anatomy and phylogenetic position of Suminia getmanovi, a basal anomodont (Amniota: Therapsida) from the Late Permian of Eastern Europe. Zoological Journal of the Linnean Society, 130:329–373.Google Scholar
Savourney, G., Launay, J.-C., Besnard, Y., Guinet, A., and Travers, S. 2003. Normo- and hypobaric hypoxia: Are there any physiological differences? European Journal of Applied Physiology, 89:122–126.Google Scholar
Sidor, C. A. 2000. Evolutionary Trends and Relationships Within the Synapsida. Unpublished Ph.D. dissertation, University of Chicago, 369 p.Google Scholar
Sidor, C. A. 2003a. Evolutionary trends and the origin of the mammalian lower jaw. Paleobiology, 29:605–640.Google Scholar
Sidor, C. A. 2003b. The naris and palate of Lycaenodon longiceps (Therapsida: Biarmosuchia), with comments on their early evolution in the Therapsida. Journal of Paleontology, 77:977–984.Google Scholar
Smith, R. and Botha, J. 2005. The recovery of terrestrial vertebrate diversity in the South African Karoo Basin after the end-Permian extinction. Comptes Rendus Palevol, 4:623–636.Google Scholar
Sues, H.-D. and Reisz, R. R. 1998. Origins and early evolution of herbivory in tetrapods. Trends in Ecology and Evolution, 13:141–145.Google Scholar
Surkov, M. V. and Benton, M. J. 2004. The basicranium of dicynodonts (Synapsida) and its use in phylogenetic analysis. Palaeontology, 47:619–638.Google Scholar
Surkov, M. V., Kalandadze, N. N., and Benton, M. J. 2005. Lystrosaurus georgi, a dicynodont from the Lower Triassic of Russia. Journal of Vertebrate Paleontology, 25:402–413.Google Scholar
Toerien, M. J. 1953. The evolution of the palate in South African Anomodontia and its classificatory significance. Palaeontologia Africana, 1:49–117.Google Scholar
Toerien, M. J. 1955. Convergent trends in Anomodontia. Evolution, 9:152–156.Google Scholar
Thulborn, T. and Turner, S. 2003. The last dicynodont: An Australian Cretaceous relict. Proceedings of the Royal Society of London Series B, 270:985–993.Google Scholar
Vega-Dias, C., Maisch, M. W., and Schultz, C. L. 2004. A new phylogenetic analysis of Triassic dicynodonts (Therapsida) and the systematics position of Jachaleria candelariensis from the Upper Triassic of Brazil. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen, 231:145–166.Google Scholar
Ward, P. D., Botha, J., Buick, R., De Kock, M. O., Erwin, D. H., Garrison, G., Kirschvink, J., and Smith, R. 2005. Abrupt and gradual extinction among Late Permian land vertebrates in the Karoo Basin, South Africa. Science, 307:709–714.Google Scholar