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Phylogenetic evidence for and implications of a dual origin of propaliny in anomodont therapsids (Synapsida)

Published online by Cambridge University Press:  08 February 2016

Kenneth D. Angielczyk*
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720

Abstract

Anomodont therapsids were the most diverse and abundant group of terrestrial vertebrate herbivores during the Late Permian and much of the Triassic. Their success has been widely attributed to a complex mastication system that was based on a propalinal sliding of the lower jaw. Traditionally, anomodont phylogeny has been viewed as an essentially linear sequence of taxa, each with more specializations for propaliny, culminating in the radiation of the dicynodont anomodonts. However, recent phylogenetic work has shown that similar specializations for propaliny can be found in members of two distinct anomodont clades, the endemic Russian Venyukovioidea and the unnamed clade consisting of Galeops + Dicynodontia. These specializations have been inferred to be present in the common ancestor of the venyukovioids and dicynodonts, implying a single origin of propaliny in anomodonts. Here a reevaluation of the anomodont feeding system is presented, and the possibility that propaliny evolved twice within the group is specifically addressed. First, I examine current hypotheses regarding anomodont phylogeny, using a modified version of data sets presented by previous authors. Then I consider the evolution of four characters related to propaliny in the context of the resulting phylogeny. The results of this investigation suggest that a dual origin of propaliny within anomodonts is not unlikely, but it depends largely on the interpretation of equivocal or poorly preserved features in some critical taxa, especially Otsheria. Given that the power stroke of mastication in basal synapsids involved the application of a posterodorsally directed force on the lower jaw, the evolution of propaliny in basal synapsids may not have been difficult. Furthermore, the independent evolution of propaliny in several other nonmammalian synapsid clades (e.g., Edaphosauria, Gorgonopsia) suggests that homoplasy may be the rule rather than the exception for this feature. Finally, the possibility of a dual origin of propaliny in anomodonts has important implications for the more general problem of the evolution of herbivory in terrestrial vertebrates. In particular, it suggests that propaliny alone was not enough to guarantee success as a herbivore during the late Paleozoic and early Mesozoic.

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References

Literature Cited

Angielczyk, K. D. 2001. Preliminary phylogenetic analysis and stratigraphic congruence of the dicynodont anomodonts (Synapsida: Therapsida). Palaeontologia Africana 37:5379.Google Scholar
Angielczyk, K. D., and Kurkin, A. A. 2003. Has the utility of Dicynodon for Upper Permian terrestrial biostratigraphy been overstated? Geology 31:363366.2.0.CO;2>CrossRefGoogle Scholar
Barghusen, H. R. 1968. The lower jaw of cynodonts (Reptilia, Therapsida) and the evolutionary origin of mammal-like adductor jaw musculature. Postilla 116:149.Google Scholar
Barghusen, H. R. 1973. The adductor jaw musculature of Dimetrodon (Reptilia, Pelycosauria). Journal of Paleontology 47:823834.Google Scholar
Barghusen, H. R. 1976. Notes on the adductor jaw musculature of Venjukovia, a primitive anomodont therapsid from the Permian of the U.S.S.R. Annals of the South African Museum 69:249260.Google Scholar
Battail, B. 2000. A comparison of Late Permian Gondwanan and Laurasian amniote faunas. Journal of African Earth Sciences 31:165174.CrossRefGoogle Scholar
Battail, B., and Surkov, M. V. 2000. Mammal-like reptiles from Russia. Pp. 120139in 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
Berman, D. S., and Sumida, S. S. 1995. New cranial material of the rare diadectid Desmatodon hesperis (Diadectomorpha) from the Late Pennsylvanian of central Colorado. Annals of the Carnegie Museum 64:315336.CrossRefGoogle Scholar
Berman, D. S., Henrici, A. C., and Sumida, S. S. 1998. Taxonomic status of the Early Permian Helodectes paridens Cope (Diadectidae) with discussions of occlusion of diadectid marginal dentitions. Annals of the Carnegie Museum 67:181196.CrossRefGoogle Scholar
Boonstra, L. D. 1965. The skull of Struthiocephalus kitchingi. Annals of the South African Museum 48:251265.Google Scholar
Bramble, D. M. 1974. Occurrence and significance of the Os transiliens in gopher tortoises. Copeia 1974:102109.CrossRefGoogle Scholar
Bremer, K. 1988. The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795803.CrossRefGoogle ScholarPubMed
Brinkman, D. 1981. The structure and relationships of the dromasaurs (Reptilia; Therapsida). Breviora 465:134.Google Scholar
Brooks, D. R., and McLennan, D. A. 1991. Phylogeny, ecology, and behavior. University of Chicago Press, Chicago.Google Scholar
Butler, P. M., and MacIntyre, G. T. 1994. Review of the British Haramiyidae (?Mammalia, Allotheria), their molar occlusion and relationships. Philosophical Transactions of the Royal Society of London B 345:433458.Google Scholar
Cheng, Z., and Li, J. 1997. A new genus of primitive dinocephalian—the third report on Late Permian Dashankou lower tetrapod fauna. Vertebrata Palasiatica 35:3543.Google Scholar
Cluver, M. A. 1970. The palate and mandible in some specimens of Dicynodon testudirostris Broom and Haughton (Reptilia, Therapsida). Annals of the South African Museum 56:133153.Google Scholar
Cluver, M. A. 1974. The cranial morphology of the Lower Triassic dicynodont Myosaurus gracilis. Annals of the South African Museum 66:3554.Google Scholar
Cluver, M. A. 1975. A new dicynodont reptile from the Tapinocephalus Zone (Karoo System, Beaufort Series) of South Africa, with evidence of the jaw adductor musculature. Annals of the South African Museum 67:723.Google Scholar
Cox, C. B. 1972. A new digging dicynodont from the Upper Permian of Tanzania. Pp. 173189in Joysey, K. A. and Kemp, T. S., eds. Studies in vertebrate evolution. Oliver and Boyd, Edinburgh.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 122:349384.CrossRefGoogle Scholar
Crompton, A. W. 1972. Postcanine occlusion in cynodonts and tritylodontids. Bulletin of the British Museum of Natural History (Geology) 21:2971.Google Scholar
Crompton, A. W., and Hotton, N., 1967. Functional morphology of the masticatory apparatus of two dicynodonts (Reptilia, Therapsida). Postilla 109:151.Google Scholar
Cunningham, C. W. 1999. Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Systematic Biology 48:665674.CrossRefGoogle Scholar
Dodick, J. T., and Modesto, S. P. 1995. The cranial anatomy of the captorhinid reptile Labidosauikos meachami from the Lower Permian of Oklahoma. Palaeontology 38:687711.Google Scholar
Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783791.CrossRefGoogle ScholarPubMed
Frumhoff, P. C., and Reeve, H. K. 1994. Using phylogenies to test hypotheses of adaptation: a critique of some current proposals. Evolution 48:172180.CrossRefGoogle ScholarPubMed
Goldman, N., Anderson, J. P., and Rodrigo, A. G. 2000. Likelihood-based tests of topologies in phylogenetics. Systematic Biology 49:652670.CrossRefGoogle ScholarPubMed
Golubev, V. K. 2000. The faunal assemblages of Permian terrestrial vertebrates from Eastern Europe. Paleontological Journal 34(Suppl. 2):S211S224.Google Scholar
Gorniak, G. C., Rosenthal, H. I., and Gans, C. 1982. Mastication in the tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia): structure and activity of the motor system. Journal of Morphology 171:321353.CrossRefGoogle ScholarPubMed
Hopson, J. A. 1991. Systematics of the nonmammalian Synapsida and implications for patterns of evolution in synapsids. Pp. 635693in Schultze, H.-P. and Trueb, L., eds. Origins of the higher groups of tetrapods. Comstock, Ithaca, N.Y.Google Scholar
Hopson, J. A., and Barghusen, H. R. 1986. An analysis of therapsid relationships. Pp. 83106in Hotton, N., MacLean, P. D., Roth, J. J., and Roth, E. C., eds. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington D.C.Google Scholar
Hotton, N., Olson, E. C., and Beerbower, R. 1997. Amniote origins and the discovery of herbivory. Pp. 207264in Sumida, S. S. and Martin, K. L. M., eds. Amniote origins. Academic Press, San Diego.Google Scholar
Hotton, N. 1986. Dicynodonts and their role as primary consumers. Pp. 7182in Hotton, N., MacLean, P. D., Roth, J. J., and Roth, E. C., eds. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, D.C.Google Scholar
Ivakhnenko, M. F. 1990. The late Paleozoic faunal assemblage of tetrapods from deposits of the Mezen' River Basin. Paleontological Journal 24:7684.Google Scholar
Ivakhnenko, M. F. 1994. A new Late Permian dromasaurian (Anomodontia) from Eastern Europe. Paleontological Journal 28:96103.Google Scholar
Ivakhnenko, M. F. 1996. Primitive anomodonts, venyukoviids, from the Late Permian of Eastern Europe. Paleontological Journal 30:575582.Google Scholar
Ivakhnenko, M. F. 2001. The tetrapods of the east European placket, the late Paleozoic territorial-natural complex. Trudy Paleontologischeskogo Instituta RAN 283:1200.Google Scholar
Ivakhnenko, M. F. 2003. The features of the lower jaw articulation in the gorgonopsian Suchogorgon (Therapsida). Paleontological Journal 37:4852.Google Scholar
Kemp, T. S. 1969. On the functional morphology of the gorgon-opsid skull. Philosophical Transactions of the Royal Society of London B 256:183.Google Scholar
Kemp, T. S. 1972. The jaw articulation and musculature of the whaitsiid Therocephalia. Pp. 213230in Joysey, K. A. and Kemp, T. S., eds. Studies in vertebrate evolution. Oliver and Boyd, Edinburgh.Google Scholar
Kemp, T. S. 1982. Mammal-like reptiles and the origin of mammals. Academic Press, London.Google Scholar
King, G. M. 1988. Anomodontia. In Wellnhofer, P., ed. Handbuch der Paläoherpetologie, Vol. 17C. Fischer, Stuttgart.Google Scholar
King, G. M. 1990. The dicynodonts: a study in paleobiology. Chapman and Hall, London.Google Scholar
King, G. M. 1993. How many species of Diictodon were there? Annals of the South African Museum 102:303325.Google Scholar
King, G. M. 1994. The early anomodont Venjukovia and the evolution of the anomodont skull. Journal of Zoology 232:351673.CrossRefGoogle Scholar
King, G. M. 1996. Reptiles and herbivory. Chapman and Hall, London.Google Scholar
King, G. M., and Cluver, M. A. 1991. The aquatic Lystrosaurus: an alternative lifestyle. Historical Biology 4:323341.CrossRefGoogle Scholar
King, G. M., Oelofsen, B. W., and Rubidge, B. S. 1989. The evolution of the dicynodont feeding system. Zoological Journal of the Linnean Society 96:185211.CrossRefGoogle Scholar
Krause, D. J. 1982. Jaw movement, dental function, and diet in the Paleocene multituberculate Ptilodus. Paleobiology 8:2652811CrossRefGoogle Scholar
Laurin, M. 1998. New data on the cranial anatomy of Lycaenops (Synapsida, Gorgonopsidae), and reflections on the possible presence of streptostyly in gorgonopsians. Journal of Vertebrate Paleontology 18:765776.CrossRefGoogle Scholar
Lee, M. Y. S., and Shine, R. 1998. Reptilian viviparity and Dollo's law. Evolution 52:14411450.CrossRefGoogle ScholarPubMed
Li, J., and Cheng, Z. 1997. First discovery of eotitanosuchian (Therapsida, Synapsida) of China. Vertebrate Palasiatica 34:268282.Google Scholar
Loock, J. C., Brynard, H. J., Heard, R. G., Kitching, J. W., and Rubidge, B. S. 1994. The stratigraphy of the lower Beaufort Group in an area south of Laingsburg, South Africa. Journal of African Earth Sciences 18:185195.CrossRefGoogle Scholar
Maddison, D. R., and Maddison, W. P. 2000. MacClade, Version 4.0. Sinauer, Sunderland, Mass.Google Scholar
Modesto, S. P. 1995. The skull of the herbivorous synapsid Edaphosaurus boanerges from the Lower Permian of Texas. Palaeontology 38:213239.Google Scholar
Modesto, S. P., and Rubidge, B. 2000. A basal anomodont therapsid from the lower Beaufort Group, Upper Permian of South Africa. Journal of Vertebrate Paleontology: 20:515521.CrossRefGoogle Scholar
Modesto, S. P., and Rybczynski, N. 2000. The amniote faunas of the Russian Permian: implications for Late Permian terrestrial vertebrate biogeography. Pp. 1734in 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 of London B 266:331337.CrossRefGoogle Scholar
Olson, E. C. 1962. Late Permian terrestrial vertebrates, U.S.A., and U.S.S.R. Transactions of the American Philosophical Society, new series 52:1224.CrossRefGoogle Scholar
Olson, E. C., and Beerbower, J. R. 1953. The San Angelo Formation, Permian of Texas, and its vertebrates. Journal of Geology 61:389423.CrossRefGoogle Scholar
Omland, K. E. 1997. Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks (Anatini). Evolution 51:16361646.CrossRefGoogle ScholarPubMed
Omland, K. E. 1999. The assumptions and challenges of ancestral state reconstructions. Systematic Biology 48:604611.CrossRefGoogle Scholar
Orlov, Y. A. 1958. The carnivorous dinocephalians of the Isheevo fauna (titanosuchians). Trudy Paleontologischeskogo Instituta, Academia Nauk S.S.S.R. 72:1114.Google Scholar
Parrington, F. R. 1955. On the cranial anatomy of some gorgonopsians and the synapsid middle ear. Proceedings of the Zoological Society of London 125:140.CrossRefGoogle Scholar
Pearson, H. S. 1924. The skull of the dicynodont reptile Kannemeyeria. Proceedings of the Zoological Society of London 1924:793826.CrossRefGoogle Scholar
Reisz, R. R. 1986. Pelycosauria. In Wellnhofer, P., ed. Handbuch der Paläoherpetologie, Vol. 17A. Fischer, Stuttgart.Google Scholar
Reisz, R. R., and Sues, H.-D. 2000. Herbivory in late Paleozoic and Triassic terrestrial vertebrates. Pp. 941in Sues, H.-D., ed. Evolution of herbivory in terrestrial vertebrates: perspectives from the fossil record. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Renaut, A. J. 2001. Dicynodont jaw mechanisms reconsidered: the Kannemeyeria (Anomodontia Therapsida) masticatory cycle. Asociación Paleontológica Argentina Publicación Especial 7:167170.Google Scholar
Ricqlès, A. de, and Taquet, P. 1982. La faune de vertebras de Permian Supérieur du Niger. I. Le captorhinomorphe Moradisaurus grandis (Reptilia, Cotylosauria)—le crane. Annales de Paléontologie 68:33106.Google Scholar
Romer, A. S., and Price, L. I. 1940. Review of the Pelycosauria. Geological Society of America Special Paper 28:1538.CrossRefGoogle Scholar
Rubidge, B. S., ed. 1995. Biostratigraphy of the Beaufort Group (Karoo Supergroup). South African Committee for Stratigraphy, Biostratigraphic Series 1:146.Google Scholar
Rubidge, B. S., and Hopson, J. A. 1990. A new anomodont therapsid from South Africa and its bearing on the ancestry of Dicynodontia. South African Journal of Science 86:4345.Google Scholar
Rubidge, B. S., and Hopson, J. A. 1996. A primitive anomodont therapsid from the base of the Beaufort Group (Upper Permian) of South Africa. Zoological Journal of the Linnean Society 117:115139.CrossRefGoogle Scholar
Rubidge, B. S., and Sidor, C. A. 2001. Evolutionary patterns among Permo-Triassic therapsids. Annual Review of Ecology and Systematics 32:440480.CrossRefGoogle Scholar
Rubidge, B. S., and van den Heever, J. A. 1997. Morphology and systematic position of the dinocephalian Styracocephalus platyrhynchus. Lethaia 30:157168.CrossRefGoogle 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 130:329373.CrossRefGoogle Scholar
Rybczynski, N. 2001. Unilateral chewing in a Permian herbivore. Journal of Vertebrate Paleontology 22(Suppl. to No. 3):95A.Google Scholar
Rybczynski, N., and Reisz, R. R. 2001. Earliest evidence for efficient oral processing in a terrestrial herbivore. Nature 411:684687.CrossRefGoogle Scholar
Schultz, T. R., Cocroft, R. B., and Churchill, G. A. 1996. The reconstruction of ancestral character states. Evolution 50:504511.CrossRefGoogle ScholarPubMed
Sidor, C. A. 2000. Evolutionary trends and relationships within the Synapsida. Ph.D. dissertation. University of Chicago, Chicago.Google Scholar
Sidor, C. A., and Hopson, J. A. 1995. The taxonomic status of the Upper Permian eotheriodont therapsids of the San Angelo Formation (Guadalupian), Texas. Journal of Vertebrate Paleontology 15(Suppl. to No. 3):53A.Google Scholar
Sigogneau-Russell, D. 1989. Theriodontia I. In Wellnohofer, P., ed. Handbuch der Paläoherpetologie, Vol. 17B.Google Scholar
Strong, E. E., and Lipscomb, D. 2000. Character coding and inapplicable data. Cladistics 15:363371.CrossRefGoogle Scholar
Sues, H.-D. 1986. The skull and dentition of two tritylodontid synapsids from the Lower Jurassic of Western North America. Bulletin of the Museum of Comparative Zoology 151:217268.Google Scholar
Sues, H.-D., and Reisz, R. R. 1998. Origins and evolution of herbivory in tetrapods. Trends in Ecology and Evolution 13:141145.CrossRefGoogle ScholarPubMed
Sullivan, C., Reisz, R. R., and Smith, R. M. H. 2002. The Permian mammal-like herbivore Diictodon, the oldest known example of sexually dimorphic armament. Proceedings of the Royal Society of London B 270:173178.CrossRefGoogle Scholar
Sushkin, P. P. 1926. Notes on the pre-Jurassic Tetrapoda from Russia. II. Contributions to the morphology and ethology of the Anomodontia. Palaeontologia Hungarica 1:328336.Google Scholar
Swofford, D. L. 2001. PAUP. Phylogenetic Analysis Using Parsimony (and Other Methods), Version 4.0b10a. Sinauer, Sunderland, Mass.Google Scholar
Tatarinov, L. P. 2000. Problems of the morphology of the theriodonts (Reptilia). Russian Journal of Herpetology 7:2940Google Scholar
Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221244.CrossRefGoogle Scholar
Throckmorton, G. S. 1976. Oral food processing in two herbivorous lizards, Iguana iguana (Iguanidae) and Uromastix aegyptius (Agamidae). Journal of Morphology 148:363390.CrossRefGoogle ScholarPubMed
Throckmorton, G. S., Hopson, J. A., and Parks, P. 1981. A redescription of Toxolophosaurus cloudi Olson, a Lower Cretaceous herbivorous sphenodontid reptile. Journal of Paleontology 55:586597.Google Scholar
Thulborn, T., and Turner, S. 2003. The last dicynodont: an Australian Cretaceous relict. Proceedings of the Royal Society of London B 270:985993.CrossRefGoogle ScholarPubMed
van den Heever, J. A. 1994. The cranial anatomy of the early Therocephalia (Amniota: Therapsida). Annale Universiteit van Stellenbosch 1994:159.Google Scholar
Wagner, P. J. 2000. Phylogenetic analyses and the fossil record: test and inferences, hypotheses and models. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective. Paleobiology 26(Suppl. to No. 4):341371.Google Scholar
Wagner, P. J. 2001. Rate heterogeneity in shell character evolution among lophospiroid gastropods. Paleobiology 27:290310.2.0.CO;2>CrossRefGoogle Scholar
Watson, D. M. S. 1912. On some reptilian jaws. Annals and Magazine of Natural History, series 8, 10:573587.CrossRefGoogle Scholar
Watson, D. M. S. 1921. The bases of classification of the Theriodontia. Proceedings of the Zoological Society of London 1921:3598.CrossRefGoogle Scholar
Watson, D. M. S. 1948. Dicynodon and its allies. Proceedings of the Zoological Society of London 118:823877.Google Scholar
Watson, D. M. S. 1954. On Bolosaurus and the origin and classification of reptiles. Bulletin of the Museum of Comparative Zoology at Harvard College 111:297449.Google Scholar
Watson, D. M. S., and Romer, A. S. 1956. A classification of therapsid reptiles. Bulletin of the Museum of Comparative Zoology at Harvard College 114:3789.Google Scholar
Weijs, W. A. 1975. Mandibular movements of the albino rat during feeding. Journal of Morphology 145:107124.CrossRefGoogle ScholarPubMed
Welles, S. P. 1941. The mandible of a diadectid cotylosaur. University of California Publications in Geological Sciences 25:423432.Google Scholar