Skip to main content Accessibility help
×
Home

Morphological innovation and the evolution of hadrosaurid dinosaurs

  • Thomas L. Stubbs (a1), Michael J. Benton (a1), Armin Elsler (a1) and Albert Prieto-Márquez (a2)

Abstract

The hadrosaurids were a successful group of herbivorous dinosaurs. During the Late Cretaceous, 100 to 66 million years ago, hadrosaurids had high diversity, rapid speciation rates, and wide geographic distribution. Most hadrosaurids were large bodied and had similar postcranial skeletons. However, they show important innovations in the skull, including disparate crests that functioned as socio-sexual display structures, and a complex feeding apparatus, with specialized jaws bearing dental batteries. Little is known about the macroevolutionary processes that produced these evolutionary novelties. Here we provide novel perspectives using evolutionary rate and disparity analyses. Our results show that hadrosaurid cranial evolution was complex and dynamic, but their postcranial skeleton and body size were conservative. High cranial disparity was achieved through multiple bursts of phenotypic innovation. We highlight contrasting evolutionary trends within hadrosaurids between the disparate facial skeleton and crests, which both showed multiple high-rate shifts, and the feeding apparatus, which had low variance and high rates on a single phylogenetic branch leading to the diverse Saurolophidae. We reveal that rapid evolutionary rates were important for producing the high disparity of exaggerated crests and present novel evidence that the hadrosaurid diversification was linked to both a key adaptive innovation in the feeding apparatus and multiple bursts of innovation in socio-sexual displays.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Morphological innovation and the evolution of hadrosaurid dinosaurs
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Morphological innovation and the evolution of hadrosaurid dinosaurs
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Morphological innovation and the evolution of hadrosaurid dinosaurs
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Footnotes

Hide All
*

Present address: Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Carrer de l'Escola Industrial 23, 08201 Sabadell, Spain. E-mail: albert.prieto@icp.cat

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.0dt2h6c

Footnotes

References

Hide All
Baker, J., Meade, A., Pagel, M., and Venditti, C.. 2016. Positive phenotypic selection inferred from phylogenies. Biological Journal of the Linnean Society 118:95115.
Bapst, D. W. 2014. Assessing the effect of time-scaling methods on phylogeny-based analyses in the fossil record. Paleobiology 40:331351.
Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Review of Earth and Planetary Sciences 42:207230.
Bell, P., Fanti, F., Currie, P., and Arbour, V.. 2014. A mummified duck-billed dinosaur with a soft-tissue cock's comb. Current Biology 24:7075.
Bell, P. R., Snively, E., and Shychoski, L.. 2009. A comparison of the jaw mechanics in hadrosaurid and ceratopsid dinosaurs using finite element analysis. Anatomical Record 292:13381351.
Benjamini, Y., and Hochberg, Y.. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57:289300.
Benson, R. B. J., Campione, N. E., Carrano, M. T., Mannion, P. D., Sullivan, C., Upchurch, P., and Evans, D.C.. 2014. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biology 12:e1001853. doi: 10.1371/journal.pbio.1001853.
Benson, R. B. J., Hunt, G., Carrano, M. T., and Campione, N.. 2018. Cope's rule and the adaptive landscape of dinosaur body size evolution. Palaeontology 61:1348.
Benton, M. J. 2015. Exploring macroevolution using modern and fossil data. Proceedings of the Royal Society of London B 282:20150569. doi: 10.1098/rspb.2015.0569.
Brett-Surman, M. K., and Wagner, J. R.. 2007. Discussion of character analysis of the appendicular anatomy in Campanian and Maastrichtian North American hadrosaurids—variation and ontogeny. Pp. 135169 in Carpenter, K., ed. Horns and beaks: ceratopsian and ornithopod dinosaurs. Indiana University Press, Bloomington.
Briggs, D. E. G., Fortey, R. A., and Wills, M. A.. 1992. Morphological disparity in the Cambrian. Science 256:16701673.
Brown, C., and Henderson, D.. 2015. A new horned dinosaur reveals convergent evolution in cranial ornamentation in Ceratopsidae. Current Biology 25:16411648.
Brusatte, S. L., Lloyd, G. T., Wang, S. C., and Norell, M. A.. 2014. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Current Biology 24:23862392.
Butler, R. J., Barrett, P. M., Kenrick, P., and Penn, M. G.. 2009. Diversity patterns amongst herbivorous dinosaurs and plants during the Cretaceous: implications for hypotheses of dinosaur/angiosperm co-evolution. Journal of Evolutionary Biology 22:446459.
Butler, R. J., Liyong, J., Jun, C., and Godefroit, P.. 2011. The postcranial osteology and phylogenetic position of the small ornithischian dinosaur Changchunsaurus parvus from the Quantou Formation (Cretaceous: Aptian–Cenomanian) of Jilin Province, north-eastern China. Palaeontology 54:667683.
Cailliez, F. 1983. The analytical solution of the additive constant problem. Psychometrika 48:305308.
Carrano, M. T. 2006. Body size evolution in the Dinosauria. Pp. 225268 in Carrano, M. T., Gaudin, T. J., Blob, R. W., and Wible, J. R., eds. Amniote paleobiology: perspectives on the evolution of mammals, birds, and reptiles. University of Chicago Press, Chicago, Ill.
Chin, K., Feldmann, R. M., and Tashman, J. N.. 2017. Consumption of crustaceans by megaherbivorous dinosaurs: dietary flexibility and dinosaur life history strategies. Scientific Reports 7:11163. doi: 10.1038/s41598-017-11538-w.
Close, R. A., Friedman, M., Lloyd, G. T., and Benson, R. B. J.. 2015. Evidence for a mid-Jurassic adaptive radiation in mammals. Current Biology 25:21372142.
Cooney, C. R., Bright, J. A., Capp, E. J. R., Chira, A. M., Hughes, E. C., Moody, C. J. A., Nouri, L. O., Varley, Z. K., and Thomas, G. H.. 2017. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542:344347.
Cruzado-Caballero, P., Fortuny, J., Llacer, S., and Canudo, J. I. 2015. Paleoneuroanatomy of the European lambeosaurine dinosaur Arenysaurus ardevoli. PeerJ 3:e802. doi: 10.7717/peerj.802.
Cuthbertson, R. S., Tirabasso, A., Rybczynski, N., and Holmes, R. B.. 2012. Kinetic limitations of intracranial joints in Brachylophosaurus canadensis and Edmontosaurus regalis (Dinosauria: Hadrosauridae), and their implications for the chewing mechanics of hadrosaurids. Anatomical Record 295:968979.
Dalla Vecchia, F. M. 2009. Tethyshadros insularis, a new hadrosauroid dinosaur (Ornithischia) from the Upper Cretaceous of Italy. Journal of Vertebrate Paleontology 29:11001116.
Dodson, P., Forster, C. A., and Sampson, S. D.. 2004 Ceratopsidae. Pp. 494513 in Weishampel, D. B., Dodson, P., and Osmolska, H., eds. The Dinosauria. University of California Press, Berkeley.
Erickson, G. M., Krick, B. A, Hamilton, M., Bourne, G. R., Norell, M. A., Lilleodden, E., and Sawyer, W. G.. 2012. Complex dental structure and wear biomechanics in hadrosaurid dinosaurs. Science 338:98101.
Erickson, G. M., Sidebottom, M. A., Kay, D. I., Turner, K. T., Ip, N., Norell, M. A., Sawyer, W. G., and Krick, B. A.. 2015. Wear biomechanics in the slicing dentition of the giant horned dinosaur Triceratops. Science Advances 1:e1500055. doi: 10.1126/sciadv.1500055.
Evans, D. C. 2010. Cranial anatomy and systematics of Hypacrosaurus altispinus, and a comparative analysis of skull growth in lambeosaurine hadrosaurids (Dinosauria: Ornithischia). Zoological Journal of the Linnean Society 159:398434.
Evans, D. C., Ridgely, R., and Witmer, L. M.. 2009. Endocranial anatomy of lambeosaurine hadrosaurids (Dinosauria: Ornithischia): a sensorineural perspective on cranial crest function. Anatomical Record 292:13151337.
Foote, M. 1997. The evolution of morphological diversity. Annual Review of Ecology, Evolution, and Systematics 28:129152.
Gates, T. A., Organ, C., and Zanno, L. E.. 2016. Bony cranial ornamentation linked to rapid evolution of gigantic theropod dinosaurs. Nature Communications 7:12931.
Hedman, M. M. 2010. Constraints on clade ages from fossil outgroups. Paleobiology 36:1631.
Herrera-Flores, J. A., Stubbs, T. L., and Benton, M. J.. 2017. Macroevolutionary patterns in Rhynchocephalia: is the tuatara (Sphenodon punctatus) a living fossil? Palaeontology 60:319328.
Hone, D. W. E., Naish, D., and Cuthill, I. C.. 2011. Does mutual sexual selection explain the evolution of head crests in pterosaurs and dinosaurs? Lethaia 45:139156.
Hopkins, M. J. 2016. Magnitude versus direction of change and the contribution of macroevolutionary trends to morphological disparity. Biological Journal of the Linnean Society 118:116130.
Hopkins, M. J., and Smith, A. B.. 2015. Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution. Proceedings of the National Academy of Sciences USA 112:37583763.
Hopson, J. A. 1975. The evolution of cranial display structures in hadrosaurian dinosaurs. Paleobiology 1:2143.
Horner, J. R., Weishampel, D. B., and Forster, C. A.. 2004. Hadrosauridae. Pp. 438463 in Weishampel, D. B., Dodson, P., and Osmolska, H., eds. The Dinosauria. University of California Press, Berkeley.
Isles, T. E. 2009. The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour. Historical Biology 21:139214.
Knapp, A., Knell, R. J., Farke, A. A., Loewen, M. A., and Hone, D. W. E.. 2018. Patterns of divergence in the morphology of ceratopsian dinosaurs: sympatry is not a driver of ornament evolution. Proceedings of the Royal Society of London B 285:20180312. doi: 10.1098/rspb.2018.0312.
Knell, R. J., Naish, D., Tomkins, J. L., and Hone, D. W. E.. 2013. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution 28:3847.
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 283:1822.
Laurin, M. 2004. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 53:594622.
Leblanc, A. R. H., Reisz, R. R., Evans, D. C., and Bailleul, A. M.. 2016. Ontogeny reveals function and evolution of the hadrosaurid dinosaur dental battery. BMC Evolutionary Biology 16:152.
Lloyd, G. T. 2016. Estimating morphological diversity and tempo with discrete character-taxon matrices: implementation, challenges, progress, and future directions. Biological Journal of the Linnean Society 118:131151.
Lloyd, G. T., Davis, K. E., Pisani, D., Tarver, J. E., Ruta, M., Sakamoto, M., Hone, D. W. E., Jennings, R., and Benton, M. J.. 2008. Dinosaurs and the Cretaceous terrestrial revolution. Proceedings of the Royal Society of London B 275:24832490.
Lloyd, G. T., Wang, S. C., and Brusatte, S. L.. 2012. Identifying heterogeneity in rates of morphological evolution: discrete character change in the evolution of lungfish (Sarcopterygii; Dipnoi). Evolution 66:330348.
Lloyd, G. T., Bapst, D. W., Friedman, M., and Davis, K. E.. 2016. Probabilistic divergence time estimation without branch lengths: dating the origins of dinosaurs, avian flight and crown birds. Biology Letters 12:20160609. doi: 10.1098/rsbl.2016.0609.
Lyson, T. R., and Longrich, N. R.. 2011. Spatial niche partitioning in dinosaurs from the latest Cretaceous (Maastrichtian) of North America. Proceedings of the Royal Society of London B 278:11581164.
Maan, M. E., and Seehausen, O.. 2011. Ecology, sexual selection and speciation. Ecology Letters 14:591602.
Makovicky, P. J., Kilbourne, B. M., Sadleir, R. W., and Norell, M. A.. 2011. A new basal ornithopod (Dinosauria, Ornithischia) from the Late Cretaceous of Mongolia. Journal of Vertebrate Paleontology 31:626640.
Maia, R., Rubenstein, D. R., and Shawkey, M. D.. 2013. Key ornamental innovations facilitate diversification in an avian radiation. Proceedings of the National Academy of Sciences USA 110:1068710692.
Maiorino, L., Farke, A. A., Kotsakis, T., and Piras, P.. 2017. Macroevolutionary patterns in cranial and lower jaw shape of ceratopsian dinosaurs (Dinosauria, Ornithischia): phylogeny, morphological integration, and evolutionary rates. Evolutionary Ecology Research 18:123167.
McDonald, A. T. 2012. Phylogeny of basal iguanodonts (Dinosauria: Ornithischia): an update. PLoS ONE 7:e36745. doi: 10.1371/journal.pone.0036745.
Navarro, C. A., Martin-Silverstone, E., and Stubbs, T. L.. 2018. Morphometric assessment of pterosaur jaw disparity. Royal Society Open Science 5:172130. doi: 10.1098/rsos.172130.
Nordén, K. K., Stubbs, T. L., Prieto-Márquez, A., and Benton, M. J.. 2018. Multifaceted disparity approach reveals dinosaur herbivory flourished before the end-Cretaceous mass extinction. Paleobiology 44:118.
Norman, D. B. 2015. On the history, osteology, and systematic position of the Wealden (Hastings Group) dinosaur Hypselospinus fittoni (Iguanodontia: Styracosterna). Zoological Journal of the Linnean Society 173:92189.
Norman, D. B., and Weishampel, D. B.. 1985. Ornithopod feeding mechanisms: their bearing on the evolution of herbivory. American Naturalist 126:151164.
O'Connor, J., Wang, X., Sullivan, C., Zheng, X., Tubaro, P., Zhang, X., and Zhou, Z.. 2013. Unique caudal plumage of Jeholornis and complex tail evolution in early birds. Proceedings of the National Academy of Sciences USA 110:1740417408.
Ősi, A., Prondvai, E., Butler, R. J., and Weishampel, D. B.. 2012. Phylogeny, histology and inferred body size evolution in a new rhabdodontid dinosaur from the Late Cretaceous of Hungary. PLoS ONE 7:e44318. doi: 10.1371/journal.pone.0044318.
Pagel, M., Meade, A, and Barker, D.. 2004. Bayesian estimation of ancestral character states on phylogenies. Systematic Biology 53:673684.
Panhuis, T. M., Butlin, R., Zuk, M., and Tregenza, T.. 2001. Sexual selection and speciation. Trends in Ecology and Evolution 16:364371.
Prieto-Márquez, A. 2010a. Global phylogeny of Hadrosauridae (Dinosauria: Ornithopoda) using parsimony and Bayesian methods. Zoological Journal of the Linnean Society 159:435502.
Prieto-Márquez, A. 2010b. Global historical biogeography of hadrosaurid dinosaurs. Zoological Journal of the Linnean Society 159:503525.
Prieto-Márquez, A., and Wagner, J. R.. 2013. The “unicorn” dinosaur that wasn't: a new reconstruction of the crest of Tsintaosaurus and the early evolution of the lambeosaurine crest and rostrum. PLoS ONE 8:e82268. doi: 10.1371/journal.pone.0082268.
Prieto-Márquez, A., Wagner, J. R., Bell, P. R., and Chiappe, L. M.. 2015. The late-surviving “duck-billed” dinosaur Augustynolophus from the upper Maastrichtian of western North America and crest evolution in Saurolophini. Geological Magazine 152:225241.
Prieto-Márquez, A., Erickson, G. M., and Ebersole, J. A.. 2016. A primitive hadrosaurid from southeastern North America and the origin and early evolution of “duck-billed” dinosaurs. Journal of Vertebrate Paleontology 36:e1054495. doi: 10.1080/02724634.2015.1054495.
Rabosky, D. L. 2017. Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification. Philosophical Transactions of the Royal Society of London B 372:20160417. doi: 10.1098/rstb.2016.0417.
R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org, accessed 20 December 2018.
Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217223.
Sakamoto, M., Benton, M. J., and Venditti, C.. 2016. Dinosaurs in decline tens of millions of years before their final extinction. Proceedings of the National Academy of Sciences USA 113:50365040.
Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.
Simões, M., Breitkreuz, L., Alvarado, M., Baca, S., Cooper, J. C., Heins, L., Herzog, K., and Lieberman, B. S.. 2016. The evolving theory of evolutionary radiations. Trends in Ecology and Evolution 31:2734.
Simpson, G. G. 1953. The major features of evolution. Columbia University Press, New York.
Soul, L. C., and Friedman, M.. 2017. Bias in phylogenetic measurements of extinction and a case study of end-Permian tetrapods. Palaeontology 60:169185.
Strickson, E., Prieto-Márquez, A., Benton, M. J., and Stubbs, T. L.. 2016. Dynamics of dental evolution in ornithopod dinosaurs. Scientific Reports 6:28904. doi: 10.1038/srep28904.
Venditti, C., Meade, A., and Pagel, M.. 2011. Multiple routes to mammalian diversity. Nature 479:393396.
Wagner, C. E., Harmon, L. J., and Seehausen, O.. 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487:366369.
Walker, J. D., Geissman, J. W., Bowring, S. A., and Babcock, L. E.. 2013. The Geological Society of America geologic time scale. GSA Bulletin 125:259272.
Wang, M., and Lloyd, G. T.. 2016. Rates of morphological evolution are heterogeneous in Early Cretaceous birds. Proceedings of the Royal Society of London B 283:20160214. doi: 10.1098/rspb.2016.0214.
Weishampel, D. B. 1997. Dinosaurian cacophony. Bioscience 47:150159.
Williams, V. S., Barrett, P. M., and Purnell, M. A.. 2009. Quantitative analysis of dental microwear in hadrosaurid dinosaurs, and the implications for hypotheses of jaw mechanics and feeding. Proceedings of the National Academy of Sciences USA 106:1119411199.
Xie, W., Lewis, P. O., Fan, Y., Kuo, L., and Chen, M-H.. 2011. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology 60:150160.
Yoder, J. B., Clancey, E., Roches, S. D., Eastman, J. M., Gentry, L., Godsoe, W., Hagey, T. J., Jochimsen, D., Oswald, B. P., Robertson, J., et al. 2010. Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology 23:15811596.

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed