Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-05T09:36:49.169Z Has data issue: false hasContentIssue false
  • English
  • Français

Body size correlates with discrete-character morphological proxies

Published online by Cambridge University Press:  16 July 2020

Tom Brougham Open the ORCID record for Tom Brougham [Opens in a new window]  and
Nicolás E. Campione Open the ORCID record for Nicolás E. Campione [Opens in a new window]
Tom Brougham
Affiliation:
School of Environmental and Rural Science, University of New England, Armidale, New South Wales2351, Australia. E-mail: [email protected], [email protected]
Nicolás E. Campione
Affiliation:
School of Environmental and Rural Science, University of New England, Armidale, New South Wales2351, Australia. E-mail: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Principal coordinates analysis (PCoA) is a statistical ordination technique commonly applied to morphology-based cladistic matrices to study macroevolutionary patterns, morphospace occupation, and disparity. However, PCoA-based morphospaces are dissociated from the original data; therefore, whether such morphospaces accurately reflect body-plan disparity or extrinsic factors, such as body size, remains uncertain. We collated nine character–taxon matrices of dinosaurs together with body-mass estimates for all taxa and tested for relationships between body size and both the principal axis of variation (i.e., PCo1) and the entire set of PCo scores. The possible effects of body size on macroevolutionary hypotheses derived from ordinated matrices were tested by reevaluating evidence for the accelerated accumulation of avian-type traits indicated by a strong directional shift in PCo1 scores in hypothetical ancestors of modern birds. Body mass significantly accounted for, on average, approximately 50% and 16% of the phylogenetically corrected variance in PCo1 and all PCo scores, respectively. Along the avian stem lineage, approximately 30% of the morphological variation is attributed to the reconstructed body masses of each ancestor. When the effects of body size are adjusted, the period of accelerated trait accumulation is replaced by a more gradual, additive process. Our results indicate that even at low proportions of variance, body size can noticeably affect macroevolutionary hypotheses generated from ordinated morphospaces. Future studies should thoroughly explore the nature of their character data in association with PCoA-based morphospaces and use a residual/covariate approach to account for potential correlations with body size.

Type
Articles
Information
Paleobiology , Volume 46 , Issue 3 , August 2020 , pp. 304 - 319
Check for updates
Copyright
Copyright © 2020 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.)

Footnotes

Data available from the Dryad Digital Repository:https://doi.org/10.5061/dryad.fxpnvx0nx

References

Literature Cited

Adams, D. C., Collyer, M. L., and Kaliontzopoulou, A.. 2019. Geomorph: software for geometric morphometric analyses. R package version 3.1.0. https://cran.r-project.org/package=geomorph.Google Scholar
Anderson, P. S. L., and Friedman, M.. 2012. Using cladistic characters to predict functional variety: experiments using early gnathostomes. Journal of Vertebrate Paleontology 32:1254–1270.CrossRefGoogle Scholar
Bapst, D. W. 2012. Paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods in Ecology and Evolution 3:803–807.CrossRefGoogle Scholar
Bazzi, M., Kear, B. P., Blom, H., Ahlberg, P. E., and Campione, N. E.. 2018. Static dental disparity and morphological turnover in sharks across the end-Cretaceous mass extinction. Current Biology 28:2607–2615.e3.CrossRefGoogle ScholarPubMed
Benson, R. B. J. 2018. Dinosaur macroevolution and macroecology. Annual Review of Ecology, Evolution, and Systematics 49:379–408.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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 61:13–48.CrossRefGoogle Scholar
Brazeau, M. D. 2011. Problematic character coding methods in morphology and their effects. Biological Journal of the Linnean Society 104:489–498.CrossRefGoogle Scholar
Briggs, D. E. G., Fortey, R. A., and Wills, M. A.. 1992. Morphological disparity in the Cambrian. Science 256:1670–1673.CrossRefGoogle ScholarPubMed
Brusatte, S. L., Benton, M. J., Ruta, M., and Lloyd, G. T.. 2008a. The first 50 Myr of dinosaur evolution: macroevolutionary pattern and morphological disparity. Biology Letters 4:733–736.CrossRefGoogle Scholar
Brusatte, S. L., Benton, M. J., Ruta, M., and Lloyd, G. T.. 2008b. Superiority, competition, and opportunism in the evolutionary radiation of dinosaurs. Science 321:1485–1488.CrossRefGoogle Scholar
Brusatte, S. L., Norell, M. A., Carr, T. D., Erickson, G. M., Hutchinson, J. R., Balanoff, A. M., Bever, G. S., Choiniere, J. N., Makovicky, P. J., and Xu, X.. 2010. Tyrannosaur paleobiology: new research on ancient exemplar organisms. Science 329:1481–1485.CrossRefGoogle ScholarPubMed
Brusatte, S. L., Butler, R. J., Prieto-Márquez, A., and Norell, M. A.. 2012. Dinosaur morphological diversity and the end-Cretaceous extinction. Nature Communications 3:804.CrossRefGoogle ScholarPubMed
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 24:2386–2392.CrossRefGoogle ScholarPubMed
Budd, G. E., and Mann, R. P.. 2018. History is written by the victors: the effect of the push of the past on the fossil record. Evolution 72:2276–2291.CrossRefGoogle ScholarPubMed
Butler, R. J., Brusatte, S. L., Andres, B., and Benson, R. B. J.. 2011. How do geological sampling biases affect studies of morphological evolution in deep time? A case study of pterosaur (Reptilia: Archosauria) disparity. Evolution 66:147–162.CrossRefGoogle ScholarPubMed
Campione, N. E., and Evans, D. C.. 2011. Cranial growth and variation in edmontosaurs (Dinosauria: Hadrosauridae): implications for latest Cretaceous megaherbivore diversity in North America. PLoS ONE 6:e25186.CrossRefGoogle ScholarPubMed
Campione, N. E., and Evans, D. C.. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:60.CrossRefGoogle ScholarPubMed
Campione, N. E., Evans, D. C., Brown, C. M., and Carrano, M. T.. 2014. Body mass estimation in non-avian bipeds using a theoretical conversion to quadruped stylopodial proportions. Methods in Ecology and Evolution 5:913–923.CrossRefGoogle Scholar
Carrano, M. T., Janis, C. M., and Sepkoski, J. J. Jr. 1999. Hadrosaurs as ungulate parallels: lost lifestyles and deficient data. Acta Palaeontologica Polonica 44:237–261.Google Scholar
Cau, A. 2018. The assembly of the avian body plan: a 160-million-year long process. Bollettino della Società Paleontologica Italiana 57:1–25.Google Scholar
Chartier, M., Löfstrand, S., von Balthazar, M., Gerber, S., Jabbour, F., Sauquet, H., and Schönenberger, J.. 2017. How (much) do flowers vary? Unbalanced disparity among flower functional modules and a mosaic pattern of morphospace occupation in the order Ericales. Proceedings of the Royal Society of London B 284:20170066.Google Scholar
Cisneros, J. C., and Ruta, M.. 2010. Morphological diversity and biogeography of procolophonids (Amniota: Parareptilia). Journal of Systematic Palaeontology 8:607–625.CrossRefGoogle Scholar
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 25:2137–2142.CrossRefGoogle ScholarPubMed
Csiki, Z., Vremir, M., Brusatte, S. L., and Norell, M. A.. 2010. An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania. Proceedings of the National Academy of Sciences USA 107:15357–15361.CrossRefGoogle ScholarPubMed
Curry Rogers, K. 2005. Titanosauria: a phylogenetic overview. Pp. 50–124in Rogers, K. Curry and Wilson, J. A., eds. The sauropods: evolution and paleobiology. University of California Press, Berkeley.Google Scholar
Dray, S., and Dufour, A.-B.. 2007. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22:1–20.CrossRefGoogle Scholar
Evans, D. C., Brown, C. M., Ryan, M. J., and Tsogtbaatar, K.. 2011. Cranial ornamentation and ontogenetic status of Homalocephale calathocercos (Ornithischia: Pachycephalosauria) from the Nemegt Formation, Mongolia. Journal of Vertebrate Paleontology 31:84–92.CrossRefGoogle Scholar
Foote, M. 1992. Paleozoic record of morphological diversity in blastozoan echinoderms. Proceedings of the National Academy of Sciences USA 89:7325–7329.CrossRefGoogle ScholarPubMed
Foote, M. 1994. Morphological disparity in Ordovician–Devonian crinoids and the early saturation of morphological space. Paleobiology 20:320–344.CrossRefGoogle Scholar
Foote, M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics 28:129–152.CrossRefGoogle Scholar
Foth, C., Brusatte, S. L., and Butler, R. J.. 2012. Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria). Journal of Evolutionary Biology 25:904–915.CrossRefGoogle Scholar
Fuentes-G., J. A., Polly, P. D., Martins, E. P., 2020. A Bayesian extension of phylogenetic generalized least squares: incorporating uncertainty in the comparative study of trait relationships and evolutionary rates. Evolution 74:311–325.CrossRefGoogle ScholarPubMed
Gerber, S. 2019. Use and misuse of discrete character data for morphospace and disparity analyses. Palaeontology 62:305–319.CrossRefGoogle Scholar
Goloboff, P. A., Farris, J. S., and Nixon, K. C.. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24:774–786.CrossRefGoogle Scholar
Gower, J. C. 1971. A general coefficient of similarity and some of its properties. Biometrics 27:857–871.CrossRefGoogle Scholar
Guillot, G., and Rousset, F.. 2013. Dismantling the Mantel tests. Methods in Ecology and Evolution 4:336–344.CrossRefGoogle Scholar
Halliday, T. J. D., and Goswami, A.. 2016. Eutherian morphological disparity across the end-Cretaceous mass extinction. Biological Journal of the Linnean Society 118:152–168.CrossRefGoogle Scholar
Hawkins, J. A., Hughes, C. E., and Scotland, R. W.. 1997. Primary homology assessment, characters and character states. Cladistics 13:275–283.CrossRefGoogle Scholar
Hetherington, A. J., Sherratt, E., Ruta, M., Wilkinson, M., Deline, B., and Donoghue, P. C. J.. 2015. Do cladistic and morphometric data capture common patterns of morphological disparity? Palaeontology 58:393–399.CrossRefGoogle Scholar
Hopkins, M. J., and Gerber, S.. 2017. Morphological disparity. Pp. 1–12in Nuno de la Rosa, L. and Müller, G., eds. Evolutionary developmental biology: a reference guide. Springer International, Cham, Switzerland.Google Scholar
Hopkins, M. J., and St John, K.. 2018. A new family of dissimilarity metrics for discrete character matrices that include inapplicable characters and its importance for disparity studies. Proceedings of the Royal Society of London B 285:20181784.Google ScholarPubMed
Hughes, M., Gerber, S., and Wills, M. A.. 2013. Clades reach highest morphological disparity early in their evolution. Proceedings of the National Academy of Sciences USA 110:13875–13879.CrossRefGoogle ScholarPubMed
Jolicoeur, P. 1963. The multivariate generalization of the allometry equation. Biometrics 19:497–499.CrossRefGoogle Scholar
Kingsolver, J. G., and Pfennig, D. W.. 2004. Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 58:1608–1612.CrossRefGoogle ScholarPubMed
Lee, M. S. Y., Cau, A., Naish, D., and Dyke, G. J.. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562–566.CrossRefGoogle Scholar
Legendre, P., and Legendre, L.. 1998. Numerical ecology, Vol. 24. Elsevier Science, Amsterdam.Google Scholar
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 118:131–151.CrossRefGoogle Scholar
Lloyd, G. T. 2018. Journeys through discrete-character morphospace: synthesizing phylogeny, tempo, and disparity. Palaeontology 61:637–645.CrossRefGoogle Scholar
Longrich, N. R., Sankey, J., and Tanke, D.. 2010. Texacephale langstoni, a new genus of pachycephalosaurid (Dinosauria: Ornithischia) from the upper Campanian Aguja Formation, southern Texas, USA. Cretaceous Research 31:274–284.CrossRefGoogle Scholar
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 44:1–18.CrossRefGoogle Scholar
O'Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B. P., Luo, Z.-X., Meng, J., Ni, X., Novacek, M. J., Perini, F. A., Randall, Z. S., Rougier, G. W., Sargis, E. J., Silcox, M. T., Simmons, N. B., Spaulding, M., Velazco, P. M., Weksler, M., Wible, J. R., and Cirranello, A. L.. 2013. The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339:662–667.CrossRefGoogle ScholarPubMed
Paradis, E., and Schliep, K.. 2019. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528.CrossRefGoogle ScholarPubMed
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., and R Core Team. 2018. Nlme: linear and nonlinear mixed effects models, R package version 3.1-137. https://CRAN.R-project.org/package=nlme.Google Scholar
Prentice, K. C., Ruta, M., and Benton, M. J.. 2011. Evolution of morphological disparity in pterosaurs. Journal of Systematic Palaeontology 9:337–353.CrossRefGoogle Scholar
Prieto-Márquez, A. 2010. Global phylogeny of Hadrosauridae (Dinosauria: Ornithopoda) using parsimony and Bayesian methods. Zoological Journal of the Linnean Society 159:435–502.CrossRefGoogle Scholar
R Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.Google Scholar
Revell, L. J. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223.CrossRefGoogle Scholar
Hackathon, R. 2019. phylobase: base package for phylogenetic structures and comparative data, R package version 0.8.6. https://CRAN.R-project.org/package=phylobase.Google Scholar
Romano, M. 2017. Disparity vs. diversity in Stegosauria (Dinosauria, Ornithischia): cranial and post-cranial sub-dataset provide different signals. Historical Biology 31:857–865.CrossRefGoogle Scholar
Ruta, M., and Wills, M. A.. 2016. Comparable disparity in the appendicular skeleton across the fish–tetrapod transition, and the morphological gap between fish and tetrapod postcrania. Palaeontology 59:249–267.CrossRefGoogle Scholar
Ruta, M., Angielczyk, K. D., Fröbisch, J., and Benton, M. J.. 2013. Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids. Proceedings of the Royal Society of London B 280:20131071.Google ScholarPubMed
Sampson, S. D., Loewen, M. A., Farke, A. A., Roberts, E. M., Forster, C. A., Smith, J. A., and Titus, A. L.. 2010. New horned dinosaurs from Utah provide evidence for intracontinental dinosaur endemism. PLoS ONE 5:e12292.CrossRefGoogle ScholarPubMed
Schliep, K. P. 2011. Phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593.CrossRefGoogle ScholarPubMed
Smith, A. J., Rosario, M. V., Eiting, T. P., and Dumont, E. R.. 2014. Joined at the hip: linked characters and the problem of missing data in studies of disparity. Evolution 68:2386–2400.Google ScholarPubMed
Sookias, R. B., Butler, R. J., and Benson, R. B. J.. 2012. Rise of dinosaurs reveals major body-size transitions are driven by passive processes of trait evolution. Proceedings of the Royal Society of London B 279:2180–2187.Google ScholarPubMed
Strickson, E., Prieto-Márquez, A., Benton, M. J., and Stubbs, T. L.. 2016. Dynamics of dental evolution in ornithopod dinosaurs. Scientific Reports 6:28904.CrossRefGoogle ScholarPubMed
Stubbs, T. L., Pierce, S. E., Rayfield, E. J., and Anderson, P. S. L.. 2013. Morphological and biomechanical disparity of crocodile-line archosaurs following the end-Triassic extinction. Proceedings of the Royal Society of London B 280:20131940.Google ScholarPubMed
Stubbs, T. L., Benton, M. J., Elsler, A., and Prieto-Márquez, A.. 2019. Morphological innovation and the evolution of hadrosaurid dinosaurs. Paleobiology 45:347–362.CrossRefGoogle Scholar
Thompson, R. S., Parish, J. C., Maidment, S. C. R., and Barrett, P. M.. 2012. Phylogeny of the ankylosaurian dinosaurs (Ornithischia: Thyreophora). Journal of Systematic Palaeontology 10:301–312.CrossRefGoogle Scholar
Thorne, P. M., Ruta, M., and Benton, M. J.. 2011. Resetting the evolution of marine reptiles at the Triassic–Jurassic boundary. Proceedings of the National Academy of Sciences USA 108:8339–8344.CrossRefGoogle ScholarPubMed
Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M., and Norell, M. A.. 2007. A basal dromaeosaurid and size evolution preceding avian flight. Science 317:1378–1381.CrossRefGoogle ScholarPubMed
Venables, W. N., and Ripley, B. D.. 2002. Modern applied statistics with S. Springer, New York.CrossRefGoogle Scholar
Wills, M. A. 1998. Crustacean disparity through the Phanerozoic: comparing morphological and stratigraphic data. Biological Journal of the Linnean Society 65:455–500.CrossRefGoogle Scholar
Wills, M. A. 2001. Morphological disparity: a primer. Pp. 55–144in Adrain, J. M., Edgecombe, G. D., and Lieberman, B. S., eds. Fossils, phylogeny, and form: an analytical approach. Springer US, Boston.CrossRefGoogle Scholar
Wills, M. A., Briggs, D. E. G., and Fortey, R. A.. 1994. Disparity as an evolutionary index: a comparison of Cambrian and Recent arthropods. Paleobiology 20:93–130.CrossRefGoogle Scholar
Wright, D. F. 2017. Phenotypic innovation and adaptive constraints in the evolutionary radiation of Palaeozoic crinoids. Scientific Reports 7:1–10.CrossRefGoogle ScholarPubMed
Young, M. T., Brusatte, S. L., Ruta, M., and Andrade, M. B. D.. 2010. The evolution of Metriorhynchoidea (Mesoeucrocodylia, Thalattosuchia): an integrated approach using geometric morphometrics, analysis of disparity, and biomechanics. Zoological Journal of the Linnean Society 158:801–859.CrossRefGoogle Scholar
Zelditch, M., Swiderski, D. L., Sheets, H. D., and Fink, W. L.. 2004. Geometric morphometrics for biologists: a primer. Elsevier Academic, Amsterdam.Google Scholar