Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T18:31:31.989Z Has data issue: false hasContentIssue false
  • English
  • Français

Recognizing sexual dimorphism in the fossil record: lessons from nonavian dinosaurs

Published online by Cambridge University Press:  27 March 2017

Jordan C. Mallon
Jordan C. Mallon*
Affiliation:
Palaeobiology, Canadian Museum of Nature, Post Office Box 3663, Station D, Ottawa, Ontario K1P 6P4, Canada. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The demonstration of sexual dimorphism in the fossil record can provide vital information about the role that sexual selection has played in the evolution of life. However, statistically robust inferences of sexual dimorphism in fossil organisms are exceedingly difficult to establish, owing to issues of sample size, experimental control, and methodology. This is particularly so in the case of dinosaurs, for which sexual dimorphism has been posited in many species, yet quantifiable data are often lacking. This study presents the first statistical investigation of sexual dimorphism across Dinosauria. It revisits prior analyses that purport to find quantitative evidence for sexual dimorphism in nine dinosaur species. After the available morphological data were subjected to a suite of statistical tests (normality and unimodality tests and mixture modeling), no evidence for sexual dimorphism was found in any of the examined taxa, contrary to conventional wisdom. This is not to say that dinosaurs were not sexually dimorphic (phylogenetic inference suggests they may well have been), only that the available evidence precludes its detection. A priori knowledge of the sexes would greatly facilitate the assessment of sexual dimorphism in the fossil record, and it is suggested that unambiguous indicators of sex (e.g., presence of eggs, embryos, medullary bone) be used to this end.

Type
Methods in Paleobiology
Information
Paleobiology , Volume 43 , Issue 3 , August 2017 , pp. 495 - 507
Copyright
Copyright © 2017 The Paleontological Society. All rights reserved 

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

Literature Cited

Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Pp. 267–281 in B. N. Petrov, and F. Csáki, eds. Proceedings of the Second International Symposium on Information Theory. Akadémiai Kiadó, Budapest.Google Scholar
Allsteadt, J., and Lang, J. W.. 1995. Sexual dimorphism in the genital morphology of young American alligators, Alligator mississippiensis . Herpetologica 51:314–325.Google Scholar
Anderson, T. W., and Darling, D. A.. 1952. Asymptotic theory of certain “goodness-of-fit” criteria based on stochastic processes. Annals of Mathematical Statistics 23:193–212.Google Scholar
Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, N.J.Google Scholar
Asher, R. J., Lin, K. H., Kardjilov, N., and Hautier, L.. 2011. Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology 24:1080–1090.Google Scholar
Barden, H. E., and Maidment, S. C. R.. 2011. Evidence for sexual dimorphism in the stegosaurian dinosaur Kentrosaurus aethiopicus from the Upper Jurassic of Tanzania. Journal of Vertebrate Paleontology 31:641–651.Google Scholar
Benton, M. J., Juul, L., Storrs, G. W., and Galton, P. M.. 2000. Anatomy and systematics of the prosauropod dinosaur Thecodontosaurus antiquus from the Upper Triassic of southwest England. Journal of Vertebrate Paleontology 20:77–108.Google Scholar
Bonnan, M. F., Farlow, J. O., and Masters, S. L.. 2008. Using linear and geometric morphometrics to detect intraspecific variability and sexual dimorphism in femoral shape in Alligator mississippiensis and its implications for sexing fossil archosaurs. Journal of Vertebrate Paleontology 28:422–431.Google Scholar
Bonucci, E., and Gherardi, G.. 1975. Histochemical and electron microscope investigations on medullary bone. Cell and Tissue Research 163:81–97.Google Scholar
Borkovic, B., and Russell, A.. 2014. Sexual selection according to Darwin: a response to Padian and Horner’s interpretation. Comptes Rendus Palevol 13:701–707.Google Scholar
Brown, B., and Schlaikjer, E. M.. 1940. The structure and relationships of Protoceratops . Annals of the New York Academy of Sciences 40:133–265.Google Scholar
Brown, B., and Schlaikjer, E. M.. 1943. A study of the troodont dinosaurs with the description of a new genus and four new species. American Museum of Natural History Bulletin 82:121–149.Google Scholar
Brown, C. M., Arbour, J. H., and Jackson, D. A.. 2012. Testing of the effect of missing data estimation and distribution in morphometric multivariate data analyses. Systematic Biology 61:941–954.Google Scholar
Bryant, H. N., and Russell, A. P.. 1992. The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society of London B 337:405–418.Google Scholar
Caldwell, M. W., and Lee, M. S. Y.. 2001. Live birth in Cretaceous marine lizards (mosasauroids). Proceedings of the Royal Society of London B 268:2397–2401.Google Scholar
Callomon, J. H. 1963. Sexual dimorphism in Jurassic ammonites. Transactions of the Leicester Literary and Philosophical Society 57:21–56.Google Scholar
Carpenter, K. 1990a. Variation in Tyrannosaurus rex. Pp. 141–145 in Carpenter and Currie 1990.Google Scholar
Carpenter, K. 1990b. Ankylosaur systematics: example using Panoplosaurus and Edmontonia (Ankylosauria: Nodosauridae). Pp. 281–298 in Carpenter and Currie 1990.Google Scholar
Carpenter, K. 1999. Eggs, nests, and baby dinosaurs: a look at dinosaur reproduction. Indiana University Press, Bloomington.Google Scholar
Carpenter, K. 2010. Variation in a population of Theropoda (Dinosauria): Allosaurus from the Cleveland-Lloyd Quarry (Upper Jurassic), Utah, USA. Paleontological Research 14:250–259.Google Scholar
Carpenter, K., and Currie, P. J., eds. 1990. Dinosaur systematics: approaches and perspectives. Cambridge University Press, Cambridge.Google Scholar
Carpenter, K., and Smith, M.. 2001. Forelimb osteology and biomechanics of Tyrannosaurus rex . Pp. 90–116 in D. H. Tanke, and K. Carpenter, eds. Mesozoic vertebrate life. Indiana University Press, Bloomington.Google Scholar
Carpenter, K., Hayashi, S., Kobayashi, Y., Maryańska, T., Barsbold, R., Sato, K., and Obata, I.. 2011. Saichania chulsanensis (Ornithischia, Ankylosauridae) from the Upper Cretaceous of Mongolia. Palaeontographica Abteilung A 294:1–61.Google Scholar
Chapman, R. E., Galton, P. M., Sepkoski, J. J. Jr., and Wall, W. P.. 1981. A morphometric study of the cranium of the pachycephalosaurid dinosaur Stegoceras . Journal of Paleontology 55:608–618.Google Scholar
Chapman, R. E., Weishampel, D. B., Hunt, G., and Raskin-Gutman, D.. 1997. Sexual dimorphism in dinosaurs. Pp. 83–93 in D. L. Wolberg, E. Stump, and G. D. Rosenberg, eds. Dinofest International: Proceedings of a Symposium Sponsored by Arizona State University. Academy of Natural Sciences, Philadelphia.Google Scholar
Cheng, Y.-N., Wu, X.-C., and Ji, Q.. 2004. Triassic marine reptiles gave birth to live young. Nature 432:383–386.Google Scholar
Cheng, Y.-N., Holmes, R., Wu, X.-C., and Alfonso, N.. 2009. Sexual dimorphism and life history of Keichousaurus hui (Reptilia: Sauropterygia). Journal of Vertebrate Paleontology 29:401–408.Google Scholar
Chinsamy, A., and Tumarkin‐Deratzian, A.. 2009. Pathologic bone tissues in a turkey vulture and a nonavian dinosaur: implications for interpreting endosteal bone and radial fibrolamellar bone in fossil dinosaurs. Anatomical Record 292:1478–1484.Google Scholar
Chinsamy, A., Chiappe, L. M., Marugán-Lobón, J., Chunling, G., and Fengjiao, Z.. 2013. Gender identification of the Mesozoic bird Confuciusornis sanctus . Nature Communications 4:1381.Google Scholar
Colbert, E. H. 1989. The Triassic dinosaur Coelophysis . Museum of Northern Arizona Bulletin 57:1–160.Google Scholar
Colbert, E. H. 1990. Variation in Coelophysis bauri. Pp. 81–90 in Carpenter and Currie 1990.Google Scholar
Cunningham, J. T. 1900. Sexual dimorphism in the animal kingdom: a theory of the evolution of secondary sexual characters. Adam and Charles Black, London.Google Scholar
Currie, P. J., and Russell, D. A.. 1988. Osteology and relationships of Chirostenotes pergracilis (Saurischia, Theropoda) from the Judith River (Oldman) Formation of Alberta, Canada. Canadian Journal of Earth Sciences 25:972–986.Google Scholar
Currie, P. J., Rigby, J. K. Jr., and Sloan, R. E.. 1990. Theropod teeth from the Judith River Formation of southern Alberta, Canada. Pp. 107–125 in Carpenter and Currie 1990.CrossRefGoogle Scholar
Currie, P. J., Langston, W. Jr., and Tanke, D. H.. 2008. A new species of Pachyrhinosaurus (Dinosauria, Ceratopsidae) from the Upper Cretaceous of Alberta, Canada. Pp. 1–108 in P. J. Currie, W. Langston, Jr., and D. H. Tanke, eds. A new horned dinosaur from an Upper Cretaceous bone bed in Alberta. NRC Research Press, Ottawa.Google Scholar
Danforth, C. H. 1930. Numerical variation and homologies in vertebrae. American Journal of Physical Anthropology 14:463–481.Google Scholar
Darwin, C. 1871. The descent of man, and selection in relation to sex. J. Murray, London.Google Scholar
Deng, T. 2005. New discovery of Iranotherium morgani (Perissodactyla, Rhinocerotidae) from the late Miocene of the Linxia Basin in Gansu, China, and its sexual dimorphism. Journal of Vertebrate Paleontology 25:442–450.Google Scholar
Dodson, P. 1975. Taxonomic implications of relative growth in lambeosaurine hadrosaurs. Systematic Biology 24:37–54.Google Scholar
Dodson, P. 1976. Quantitative aspects of relative growth and sexual dimorphism in Protoceratops . Journal of Paleontology 50:929–940.Google Scholar
Dodson, P. 1990. On the status of the ceratopsids Monoclonius and Centrosaurus. Pp. 231–243 in Carpenter and Currie 1990.Google Scholar
Dodson, P. 2011. Sex in the Cretaceous—how to tell the girls from the boys. American Paleontologist 19(3):21–24.Google Scholar
Dong, Z. 1997. Mixture analysis and its preliminary application in archaeology. Journal of Archaeological Science 24:141–161.Google Scholar
Evans, D. C. 2007. Ontogeny and evolution of lambeosaurine dinosaurs (Ornithischia: Hadrosauridae). Unpublished Ph.D. dissertation. University of Toronto, Toronto.Google Scholar
Farlow, J. O. 1990. Review: dynamic dinosaurs. Paleobiology 16:234–241.Google Scholar
Galton, P. M. 1982a. Juveniles of the stegosaurian dinosaur Stegosaurus from the Upper Jurassic of North America. Journal of Vertebrate Paleontology 2:47–62.Google Scholar
Galton, P. M. 1982b. The postcranial anatomy of stegosaurian dinosaur Kentrosaurus from the upper Jurassic of Tanzania, East Africa. Geologica et Palaeontologica 15:139–160.Google Scholar
Galton, P. M. 1985. British plated dinosaurs (Ornithischia, Stegosauridae). Journal of Vertebrate Paleontology 5:211–254.Google Scholar
Galton, P. M. 1990. Stegosauria. Pp. 435–455 in D. B. Weishampel, P. Dodson, and H. Osmólska, eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Galton, P. M. 1991. Postcranial remains of stegosaurian dinosaur Dacentrurus armatus from upper Jurassic of France and Portugal. Geologica et Palaeontologica 25:299–327.Google Scholar
Galton, P. M. 1997. Comments on sexual dimorphism in the prosauropod dinosaur Plateosaurus engelhardti (Upper Triassic, Trossingen). Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 1997:674–682.CrossRefGoogle Scholar
Galton, P. M. 1999. Sex, sacra and Sellosaurus gracilis (Saurischia, Sauropodomorpha, Upper Triassic, Germany)—or why the character “two sacral vertebrae” is plesiomorphic for Dinosauria. Neues Jahrbuch fur Geologie und Palaontologie-Abhandlungen 213:19–56.Google Scholar
Galton, P. M., and Upchurch, P.. 2004. Stegosauria. Pp. 343–362 in D. B. Weishampel, P. Dodson, and H. Osmólska, eds. The Dinosauria, 2nd ed. University of California Press, Berkeley.Google Scholar
Gangloff, R. A. 1995. Edmontonia sp., the first record of an ankylosaur from Alaska. Journal of Vertebrate Paleontology 15:195–200.Google Scholar
Gingerich, P. 1981. Cranial morphology and adaptations in Eocene Adapidae. 1. Sexual dimorphism in Adapis magnus and Adapis parisiensis . American Journal of Physical Anthropology 56:217–234.Google Scholar
Godfrey, L. R., Lyon, S. K., and Sutherland, M. R.. 1993. Sexual dimorphism in large-bodied primates: the case of the subfossil lemurs. American Journal of Physical Anthropology 90:315–334.Google Scholar
Goodwin, W. B. 1990. Morphometric landmarks of pachycephalosaurid cranial material from the Judith River Formation of northcentral Montana. Pp. 189–201 in Carpenter and Currie 1990.CrossRefGoogle Scholar
Gow, C. E., Kitching, J. W., and Raath, M. A.. 1990. Skulls of the prosauropod dinosaur Massospondylus carinatus Owen in the collections of the Bernard Price Institute for Palaeontological Research. Palaeontologia africana 27:45–58.Google Scholar
Goymann, W., Makomba, M., Urasa, F., and Schwabl, I.. 2015. Social monogamy vs. polyandry: ecological factors associated with sex roles in two closely related birds within the same habitat. Journal of Evolutionary Biology 28:1335–1353.Google Scholar
Gregory, W. K., and Mook, C. C.. 1925. On Protoceratops, a primitive ceratopsian dinosaur from the Lower Cretaceous of Mongolia. American Museum Novitates 156:1–9.Google Scholar
Gross, J., and Ligges, U.. 2015. nortest: tests for normality. R package, Version 1:0–4.Google Scholar
Hammer, Ø., and Harper, D. A.. 2001. Paleontological data analysis. Blackwell Publishing: Malden, Mass.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D.. 2001. PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 4(1):1–9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.Google Scholar
Handa, N., Watabe, M., and Tsogtbaatar, K.. 2012. New specimens of Protoceratops (Dinosauria: Neoceratopsia) from the Upper Cretaceous in Udyn Sayr, southern Gobi area, Mongolia. Paleontological Research 16:179–198.Google Scholar
Handley, W. D., Chinsamy, A., Yates, A. M., and Worthy, T. H.. 2016. Sexual dimorphism in the late Miocene mihirung Dromornis stirtoni (Aves: Dromornithidae) from the Alcoota Local Fauna of central Australia. Journal of Vertebrate Paleontology 36:e1180298. doi: 10.1080/02724634.2016.1180298.Google Scholar
Hartigan, J. A., and Hartigan, P. M.. 1985. The dip test of unimodality. Annals of Statistics 13:70–84.Google Scholar
Hedrick, A. V., and Temeles, E. J.. 1989. The evolution of sexual dimorphism in animals: hypotheses and tests. Trends in Ecology and Evolution 4:136–138.CrossRefGoogle ScholarPubMed
Hone, D. W., Naish, D., and Cuthill, I. C.. 2012. Does mutual sexual selection explain the evolution of head crests in pterosaurs and dinosaurs? Lethaia 45:139–156.Google Scholar
Hone, D. W., Farke, A. A., and Wedel, M. J.. 2016a. Ontogeny and the fossil record: what, if anything, is an adult dinosaur? Biology Letters 12:20150947. doi: 10.1098/rsbl.2015.0947.Google Scholar
Hone, D. W., Wood, D., and Knell, R. J.. 2016b. Positive allometry for exaggerated structures in the ceratopsian dinosaur Protoceratops andrewsi supports socio-sexual signaling. Palaeontologia Electronica 19(1):1–13.Google Scholar
Hopson, J. A. 1975. The evolution of cranial display structures in hadrosaurian dinosaurs. Paleobiology 1:21–43.Google Scholar
Horner, J. R., and Padian, K.. 2004. Age and growth dynamics of Tyrannosaurus rex . Proceedings of the Royal Society of London B 271:1875–1880.Google Scholar
Hübner, T. R. 2012. Bone histology in Dysalotosaurus lettowvorbecki (Ornithischia: Iguanodontia)–variation, growth, and implications. PLoS ONE 7:e29958. doi: 10.1371/journal.pone.0029958.CrossRefGoogle ScholarPubMed
Isles, T. E. 2009. The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour. Historical Biology 21:139–214.Google Scholar
Josephson, S. C., Juell, K. E., and Rogers, A. R.. 1996. Estimating sexual dimorphism by method‐of‐moments. American Journal of Physical Anthropology 100:191–206.Google Scholar
Klein, N., and Sander, P. M.. 2007. Bone histology and growth of the prosauropod dinosaur Plateosaurus engelhardti von Meyer, 1837 from the Norian bonebeds of Trossingen (Germany) and Frick (Switzerland). Special Papers in Palaeontology 77:169–206.Google Scholar
Klein, N., and Sander, P. M.. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34:247–263.Google Scholar
Knell, R. J., and Fortey, R. A.. 2005. Trilobite spines and beetle horns: sexual selection in the Palaeozoic? Biology Letters 1:196–199.Google Scholar
Knell, R. J., and Sampson, S.. 2011. Bizarre structures in dinosaurs: species recognition or sexual selection? A response to Padian and Horner. Journal of Zoology 283:18–22.Google Scholar
Knell, R. J., Naish, D., Tomkins, J. L., and Hone, D. W.. 2013a. Is sexual selection defined by dimorphism alone? A reply to Padian and Horner. Proceedings of the Zoological Society of London 35:491–562.Google Scholar
Knell, R. J., Naish, D., Tomkins, J. L., and Hone, D. W.. 2013b. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution 28:38–47.Google Scholar
Kościński, K., and Pietraszewski, S.. 2004. Methods to estimate sexual dimorphism from unsexed samples: a test with computer-generated samples. Przegląd Antropologiczny—Anthropological Review 67:33–55.Google Scholar
Kurzanov, S. M. 1972. Sexual dimorphism in protoceratopsians. Palaeontological Journal 1:91–97.Google Scholar
Lambert, O., Godefroit, P., Li, H., Shang, C. Y., and Dong, Z.-M.. 2001. A new species of Protoceratops (Dinosauria, Neoceratopsia) from the Late Cretaceous of Inner Mongolia (PR China). Bulletin de l’Institut Royal des Sciences Naturelles de Belgique. Sciences de la Terre, Supplément 71:5–28.Google Scholar
Larson, P. L. 1994. Tyrannosaurus sex. Paleontological Society Special Publication 7:139–155.Google Scholar
Larson, P. L. 1997. The king’s new clothes: a fresh look at Tyrannosaurus rex . Pp. 65–71 in D. L. Wolberg, E. Stump, and G. D. Rosenberg, eds. Dinofest lnternational: Proceedings of a Symposium Sponsored by Arizona State University. Academy of Natural Sciences, Philadelphia.Google Scholar
Larson, P. L. 2008. Variation and sexual dimorphism in Tyrannosaurus rex . Pp. 103–128 in P. Larson, and K. Carpenter, eds. Tyrannosaurus rex: the tyrant king. Indiana University Press, Bloomington.Google Scholar
Lee, A. H., and Werning, S.. 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences of the USA 105:582–587.Google Scholar
Lehman, T. M. 1990. The ceratopsian subfamily Chasmosaurinae: sexual dimorphism and systematics. Pp. 211–229 in Carpenter and Currie 1990.Google Scholar
Livezey, B. C., and Humphrey, P. S.. 1984. Sexual dimorphism in continental steamer-ducks. Condor 86:368–377.Google Scholar
Loewen, M. A. 2009. Variation in the late Jurassic theropod dinosaur Allosaurus: ontogenetic, functional, and taxonomic implications. Unpublished Ph.D. dissertation. University of Utah, Salt Lake City.Google Scholar
Lü, J., Unwin, D., Deeming, D. C., Jin, X., Liu, Y., and Ji, Q.. 2011. An egg-adult association, gender and reproduction in pterosaurs. Science 331:321–324.Google Scholar
Maechler, M. 2015. diptest: Hartigan’s dip test statistic for unimodality—corrected R Package. Version 0:75–77.Google Scholar
Maiorino, L., Farke, A. A., Kotsakis, T., and Piras, P.. 2015. Males resemble females: re-evaluating sexual dimorphism in Protoceratops andrewsi (Neoceratopsia, Protoceratopsidae). PLoS ONE 10:e0126464. doi: 10.1371/journal.pone.0126464.Google Scholar
Mallon, J. C., and Holmes, R. B.. 2006. A reevaluation of sexual dimorphism in the postcranium of the chasmosaurine ceratopsid Chasmosaurus belli (Dinosauria: Ornithischia). Canadian Field-Naturalist 120:403–412.Google Scholar
Mendelson, T. C., and Shaw, K. L.. 2013. Further misconceptions about species recognition: a reply to Padian and Horner. Trends in Ecology and Evolution 28:252–253.Google Scholar
Nopcsa, F.. 1929. Sexual differences in ornithopodous dinosaurs. Palaeobiologica 2:187–201.Google Scholar
O’Harra, C. C. 1930. A fossil mammal with unborn twins. Science 71:341–342.Google Scholar
Padian, K., and Horner, J. R.. 2011a. The evolution of “bizarre structures” in dinosaurs: biomechanics, sexual selection, social selection or species recognition? Journal of Zoology 283:3–17.Google Scholar
Padian, K., and Horner, J. R.. 2011b. The definition of sexual selection and its implications for dinosaurian biology. Journal of Zoology 283:23–27.Google Scholar
Padian, K., and Horner, J. R.. 2013. Misconceptions of sexual selection and species recognition: a response to Knell et al. and to Mendelson and Shaw. Trends in Ecology and Evolution 28:249–250.Google Scholar
Padian, K., and Horner, J. R.. 2014a. The species recognition hypothesis explains exaggerated structures in non-avian dinosaurs better than sexual selection does. Comptes Rendus Palevol 13:97–107.Google Scholar
Padian, K., and Horner, J. R.. 2014b. Darwin’s sexual selection: understanding his ideas in context. Comptes Rendus Palevol 13:709–715.Google Scholar
Penkalski, P. 2001. Variation in specimens referred to Euoplocephalus tutus . Pp. 261–298 in K. Carpenter, ed. The armored dinosaurs. Indiana University Press, Bloomington.Google Scholar
Persons, W. S. IV, Funston, G. F., Currie, P. J., and Norell, M. A.. 2015. A possible instance of sexual dimorphism in the tails of two oviraptorosaur dinosaurs. Scientific Reports 5:9472.Google Scholar
Platt, S. G., Rainwater, T. R., Thorbjarnarson, J. B., Finger, A. G., Anderson, T. A., and McMurry, S. T.. 2009. Size estimation, morphometrics, sex ratio, sexual size dimorphism, and biomass of Morelet’s crocodile in northern Belize. Caribbean Journal of Science 45:80–93.CrossRefGoogle Scholar
Plavcan, J. M. 1994. Comparison of four simple methods for estimating sexual dimorphism in fossils. American Journal of Physical Anthropology 94:465–476.Google Scholar
Prieto-Marquez, A., Gignac, P. M., and Joshi, S.. 2007. Neontological evaluation of pelvic skeletal attributes purported to reflect sex in extinct non-avian archosaurs. Journal of Vertebrate Paleontology 27:603–609.Google Scholar
Raath, M. A. 1990. Morphological variation in small theropods and its meaning in systematics: evidence from Syntarsus. Pp. 91–105 in Carpenter and Currie 1990.CrossRefGoogle Scholar
Rinehart, L. F., Lucas, S. G., Heckert, A. B., Spielmann, J. A., and Celeskey, M. D.. 2009. The paleobiology of Coelophysis bauri (Cope) from the Upper Triassic (Apachean) Whitaker quarry, New Mexico, with detailed analysis of a single quarry block. New Mexico Museum of Natural History and Science Bulletin 45:1–260.Google Scholar
Rothschild, B. M., and Berman, D. S.. 1991. Fusion of caudal vertebrae in Late Jurassic sauropods. Journal of Vertebrate Paleontology 11:29–36.Google Scholar
Rowe, T. 1989. A new species of the theropod dinosaur Syntarsus from the Early Jurassic Kayenta Formation of Arizona. Journal of Vertebrate Paleontology 9:125–136.Google Scholar
Rozhdestvensky, A. K. 1965. Growth changes in Asian dinosaurs and some problems of their taxonomy. Paleontologičeskij Žurnal 3:95–109 [In Russian.]Google Scholar
R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org.Google Scholar
Ryan, M. J., and Evans, D. C.. 2005. Ornithischian dinosaurs. Pp. 312–348 in P. J. Currie, and E. B. Koppelhus, eds. Dinosaur Provincial Park: a spectacular ancient ecosystem revealed. Indiana University Press, Bloomington.Google Scholar
Saitta, E. T. 2015. Evidence for sexual dimorphism in the plated dinosaur Stegosaurus mjosi (Ornithischia, Stegosauria) from the Morrison Formation (Upper Jurassic) of western USA. PLoS ONE 10:e0123503. doi: 10.1371/journal.pone.0123503.CrossRefGoogle ScholarPubMed
Sanchez, I., Quiralte, V., Morales, J., Azanza, B., and Pickford, M.. 2010. Sexual dimorphism of the frontal appendages of the early Miocene African pecoran Prolibytherium Arambourg, 1961 (Mammalia, Ruminantia). Journal of Vertebrate Paleontology 30:1306–1310.Google Scholar
Sander, P. M. 2000. Long bone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466–488.Google Scholar
Sato, T., Cheng, Y.-N., Wu, X.-C., Zelenitsky, D. K., and Hsiao, Y.-F.. 2005. A pair of shelled eggs inside a female dinosaur. Science 308:375.Google Scholar
Schoener, T. W. 1967. The ecological significance of sexual dimorphism in size in the lizard Anolis conspersus . Science 155:474–477.Google Scholar
Schott, R. K., Evans, D. C., Goodwin, M. B., Horner, J. R., Brown, C. M., and Longrich, N. R.. 2011. Cranial ontogeny in Stegoceras validum (Dinosauria: Pachycephalosauria): a quantitative model of pachycephalosaur dome growth and variation. PLoS ONE 6:e21092. doi: 10.1371/journal.pone.0021092.Google Scholar
Schweitzer, M. H., Wittmeyer, J. L., and Horner, J. R.. 2005. Gender-specific reproductive tissue in ratites and Tyrannosaurus rex . Science 308:1456–1460.Google Scholar
Schweitzer, M. H., Elsey, R. M., Dacke, C. G., Horner, J. R., and Lamm, E.-T.. 2007. Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone? Bone 40:1152–1158.Google Scholar
Schweitzer, M. H., Zheng, W., Zanno, L., Werning, S., and Sugiyama, T.. 2016. Chemistry supports the identification of gender-specific reproductive tissue in Tyrannosaurus rex . Scientific Reports 6:23099.Google Scholar
Shapiro, S. S., and Wilk, M. B.. 1965. An analysis of variance test for normality (complete samples). Biometrika 52:591–611.Google Scholar
Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 64:419–461.Google Scholar
Smith, D. K. 1998. A morphometric analysis of Allosaurus . Journal of Vertebrate Paleontology 18:126–142.Google Scholar
Stacklies, W., Redestig, H., Scholz, M., Walther, D., and Selbig, J.. 2007. pcaMethods—a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167.Google Scholar
Sternberg, C. M. 1927. Horned dinosaur group in the National Museum of Canada. Canadian Field-Naturalist 41:67–73.Google Scholar
Tereshchenko, V. S. 2001. Sexual dimorphism in the postcranial skeleton of protoceratopsids (Neoceratopsia, Protoceratopsidae) from Mongolia. Paleontological Journal 35:415–425.Google Scholar
Thulborn, R. A. 1974. A new heterodontosaurid dinosaur (Reptilia: Ornithischia) from the Upper Triassic Red Beds of Lesotho. Zoological Journal of the Linnean Society of London 55:151–175.Google Scholar
Thulborn, R. A. 1994. Dimorphic jaw bones in the theropod Allosaurus fragilis . Association of Australian Palaeontologists, Sydney, Australasian Palaeontological Convention Abstracts and Programme 94:54.Google Scholar
Tomkins, J. L., LeBas, N. R., Witton, M. P., Martill, D. M., and Humphries, S.. 2010. Positive allometry and the prehistory of sexual selection. American Naturalist 176:141–148.Google Scholar
VanBuren, C. S., and Evans, D. C.. In press. Evolution and function of anterior cervical vertebral fusion in tetrapods. Biological Reviews. doi: 10.1111/brv.12245.Google Scholar
Van Valkenburgh, B., and Sacco, T.. 2002. Sexual dimorphism, social behavior, and intrasexual competition in large Pleistocene carnivorans. Journal of Vertebrate Paleontology 22:164–169.Google Scholar
Ward, P. 1965. Feeding ecology of the black‐faced dioch Quelea quelea in Nigeria. Ibis 107:173–214.CrossRefGoogle Scholar
Webb, G. J. W., and Messel, H.. 1978. Morphometric analysis of Crocodylus porosus from the north coast of Arnhem Land, northern Australia. Australian Journal of Zoology 26:1–27.Google Scholar
Weishampel, D. B. 1981. Acoustic analyses of potential vocalization in lambeosaurine dinosaurs (Reptilia: Ornithischia). Paleobiology 7:252–261.Google Scholar
Weishampel, D. B., and Chapman, R. E.. 1990). Morphometric study of Plateosaurus from Trossingen (Baden-Württemberg, Federal Republic of Germany). Pp. 43–51 in Carpenter and Currie 1990.Google Scholar
Westermann, G. E. G. ed. 1969. Sexual dimorphism in fossil Metazoa and taxonomic implications. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.Google Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33 in J. J. Thomason, ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Woodward, H. N., Freedman Fowler, E. A., Farlow, J. O., and Horner, J. R.. 2015. Maiasaura, a model organism for extinct vertebrate population biology: a large sample statistical assessment of growth dynamics and survivorship. Paleobiology 41:503–527.Google Scholar
Zelenitsky, D. K., Therrien, F., Joyce, W. G., and Brinkman, D. B.. 2008. First fossil gravid turtle provides insight into the evolution of reproductive traits in turtles. Biology Letters 4:715–718.Google Scholar