Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-18T01:32:48.551Z Has data issue: false hasContentIssue false

Multiple regression modeling for estimating endocranial volume in extinct Mammalia

Published online by Cambridge University Press:  08 April 2016

Laura C. Soul
Affiliation:
Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, U.K.
Roger B. J. Benson
Affiliation:
Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, U.K.
Vera Weisbecker
Affiliation:
Department of Earth Sciences, Downing Street, Cambridge CB2 3EQ, U.K.

Abstract

The profound evolutionary success of mammals has been linked to behavioral and life-history traits, many of which have been tied to brain size. However, studies of the evolution of this key trait have yet to explore the full potential of the fossil record, being limited by the difficulty of obtaining endocranial data from fossils. Using measurements of endocranial volume, length, height, and width of the braincase in 503 adult specimens from 199 extant species, representing 99 of 133 extant mammalian families, we expand upon a simple method of using multiple regression to develop a formula for estimating brain size from external skull measurements. We also examined non-mammalian synapsids to assess the phylogenetic limits of our model's application. Model-predicted volume correlates strongly with measured volume (R2 = 0.993) and prediction error is between 16% and 19%. Error decreases if models developed for well-sampled subclades such as primates or rodents are used, demonstrating that some differential evolution of the relationship between brain size and skull size has occurred. However, reanalysis using phylogenetically independent contrasts demonstrates weak phylogenetic dependency, indicating that our model is appropriate for estimating the endocranial volume of species of unknown phylogenetic affinity. Thus, the model represents a generally applicable, fast and cost-efficient way to dramatically expand the taxonomic and temporal scope of mammalian brain size data sets. Even endocranial volumes of taxa with highly derived crania, such as cetaceans and monotremes, can be estimated confidently. However, the model works best for generalized placental crania. Fundamental differences in cranial architecture suggest that the model cannot provide accurate estimates of endocranial volume in non-mammalian synapsids more basal than Morganucodon (ca. 200 Ma). Therefore, use of the model for taxa phylogenetically distant from the mammalian crown group is not warranted, but it might be used to establish relative brain sizes between closely related subgroups.

Type
Articles
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

Literature Cited

Aplin, K. P. 1990. Basicranial regions of diprotodontean marsupials: anatomy, ontogeny and phylogeny. Ph.D. thesis. University of New South Wales, Sydney.Google Scholar
Ashwell, K. 2008. Encephalisation of Australian and New Guinean marsupials. Brain, Behaviour and Evolution 71:181199.Google Scholar
Barton, R., and Capellini, I. 2011. Maternal investment, life histories, and the costs of brain growth in mammals. Proceedings of the National Academy of Sciences USA 108:61696174.Google Scholar
Barton, R. A., and Harvey, P. H. 2000. Mosaic evolution of brain structure in mammals. Nature 405:10551056.Google Scholar
Beck, R. M. D., Bininda-Emonds, O. R. P., Cardillo, M., Liu, F. R., and Purvis, A. 2006. A higher-level MRP supertree of placental mammals. BMC Evolutionary Biology 6:93.Google Scholar
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., and Purvis, A. 2007. The delayed rise of present-day mammals. Nature 446:507512.Google Scholar
Burnham, K. P., and Anderson, D. R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.Google Scholar
Deaner, R. O., Isler, K., Burkart, J., and van Schaik, C. 2007. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain, Behavior and Evolution 70:115124.Google Scholar
Delsuc, F., Scally, M., Stanhope, M. J., de Jong, W. W., Catzeflis, F. M., Springer, M. S., and Douzery, E. J. P. 2002. Molecular phylogeny of living xenarthrans and the impact of character and taxon sampling on the placental tree rooting. Molecular Biology and Evolution 10:16561671.Google Scholar
de Magalhães, J. P., Costa, J., and Church, G. M. 2007. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. Journals of Gerontology Series A 62:149160.Google Scholar
Dolan, K. J. 2005. Cranial suture closure in two species of South American monkeys. American Journal of Physical Anthropology 35:109117.CrossRefGoogle Scholar
Dunbar, R. I. M., and Shultz, S. 2007. Evolution in the Social Brain. Science 317:13441347.CrossRefGoogle ScholarPubMed
Edwards, A. W. F. 1992. Likelihood: expanded edition. Johns Hopkins University Press, Baltimore, Maryland.Google Scholar
Farris, S. M., and Schulmeister, S. 2011. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proceedings of the Royal Society of London B 278:940951.Google Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:115.Google Scholar
Fenart, R., and Deblock, R. 1974. Sexual differences in adult skulls of Pan troglodytes. Journal of Human Evolution 3:123133.Google Scholar
Finarelli, J. A. 2006. Estimation of cranial volume through the use of external skull measures in the Carnivora (Mammalia). Journal of Mammalogy 87:10271036.Google Scholar
Finarelli, J. A. 2008. Testing hypotheses of the evolution of brain-body size scaling in the Canidae (Carnivora, Mammalia). Paleobiology 34:3545.CrossRefGoogle Scholar
Finarelli, J. A. 2010. Does encephalization correlate with life history or metabolic rate in Carnivora? Biology Letters 6 (3):350353.Google Scholar
Finarelli, J. A. 2011. Estimating endocranial volume from the outside of the skull in Artiodactyla. Biology Letters 5:200212.Google Scholar
Finarelli, J. A., and Flynn, J. J. 2007. The evolution of encephalisation in caniform carnivorans. Evolution 61:17581772.CrossRefGoogle Scholar
Finarelli, J. A., 2009. Brain-size evolution and sociality in Carnivora. Proceedings of the National Academy of Sciences USA 106:93459349.CrossRefGoogle ScholarPubMed
Garcia, N. E., Santos, J. L., Arsuaga, J. L., and Carretero, J. M. 2007. Endocranial morphology of Ursus deningeri Von Reichenau, 1904; from the Sima de Los Huesos (Sierra de Atapuerca) middle Pleistocene site. Journal of Vertebrate Paleontology 27 (4):10071017.Google Scholar
Garland, T. Jr., and Ives, A. R. 2000. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. American Naturalist 155:346364.CrossRefGoogle ScholarPubMed
Garland, T. Jr., HarveyT., P. H. T., P. H., and Ives, A. R. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:1832.CrossRefGoogle Scholar
Garland, T. Jr., Bennett, A. F., and Rezende, E. L. 2005. Phylogenetic approaches in comparative physiology. Journal of Experimental Biology 208:30153035.Google Scholar
Goswami, A., Weisbecker, V., and Sánchez-Villagra, M. R. 2009. Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Biology Molecular and Developmental Evolution 312B:186196.Google Scholar
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of London B 326:119157.Google Scholar
Haight, J. R., and Murray, P. F. 1981. The cranial endocast of the early Miocene marsupial, Wynyardia bassiana: an assessment of taxonomic relationships based upon comparisons with recent forms. Brain, Behavior and Evolution 19:1736.CrossRefGoogle ScholarPubMed
Harvey, P. H., and Pagel, M. D. 1991. The comparative method in evolutionary biology. Oxford University Press, New York.Google Scholar
Healy, S. D., and Rowe, C. 2007. A critique of comparative studies of brain size. Proceedings of the Royal Society of London B 274:453464.Google Scholar
Helms, J. A., and Schneider, R. A. 2003. Cranial skeletal biology. Nature 423:326331.CrossRefGoogle ScholarPubMed
Huchon, D., and Douzery, E. J. P. 2001. From the old world to the new world: A molecular chronicle of the phylogeny and biogeography of hystricognath rodents. Molecular Phylogenetics and Evolution 20:238251.Google Scholar
Huchon, D., Catzeflis, F. M., and Douzery, E. J. P. 2000. Variance of molecular datings, evolution of rodents and the phylogenetic affinities between Ctenodactylidae and Hystricognathi. Proceedings of the Royal Society of London B 267:393402.Google Scholar
Huchon, D., Madsen, O., Sibbald, M. J. J. B., Ament, K., Stanhope, M. J., Catzeflis, F. M., de Jong, W. W., and Douzery, E. J. P. 2002. Rodent phylogeny and a timescale for the evolution of glires: evidence from an extensive taxon sampling using three nuclear genes. Molecular Biology and Evolution 19:10531065.Google Scholar
Isler, K., and van Schaik, C. P. 2006. Metabolic costs of brain size evolution. Biology Letters 2:557560.Google Scholar
Iwaniuk, A. N., and Nelson, J. 2002. Can endocranial volume be used as an estimate of brain size in birds? Canadian Journal of Zoology 80:1623.Google Scholar
Jerison, H. J. 1973. Evolution of brain and intelligence. Academic Press, London.Google Scholar
Jerison, H. J., and Barlow, H. B. 1985. Animal intelligence as encephalization. Philosophical Transactions of the Royal Society of London B 308:2135.Google Scholar
Kemp, T. 2006. The origin and early radiation of the therapsid mammal-like reptiles: a palaeobiological hypothesis. Journal of Evolutionary Biology 19:12311247.Google Scholar
Koepfli, K. P., Deere, K. A., Slater, G. J., Begg, C., Begg, K., Grassman, L., Lucherini, A., Veron, G., and Wayne, R. K. 2008. Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biology 6:1186.Google Scholar
Krajewski, C., Wroe, S., and Westerman, M. 2000. Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zoological Journal of the Linnean Society 130:375404.Google Scholar
Laurin, M. 2004. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 53:594622.Google Scholar
Lefebvre, L., and Sol, D. 2008. Brains, lifestyles and cognition: are there general trends. Brain, Behavior and Evolution 72:135144.Google Scholar
Lefebvre, L., Reader, S. M., and Sol, D. 2004. Brains, innovations and evolution in birds and primates. Brain, Behavior and Evolution 63:233246.Google Scholar
MacLean, E. L., Barrickman, N. L., Johnson, E. M., and Wall, C. E. 2009. Sociality, ecology, and relative brain size in lemurs. Journal of Human Evolution 56:471478.Google Scholar
Macrini, T. E., Rougier, G. W., and Rowe, T. 2007. Description of a cranial endocast from the fossil mammal Vincelestes (Theriiformes) and its relevance to the evolution of endocranial characters in Therians. Anatomical Record 290:875892.Google Scholar
Maddison, W. P., and Maddison, D. R. 2009. Mesquite: a modular system for evolutionary analysis, Version 2.71. http://mesquiteproject.org.Google Scholar
Marino, L. 1998. A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain, Behavior and Evolution 51:230238.Google Scholar
Marino, L., Uhen, M. D., Frohlich, B., Aldag, J. M., Blane, C., Bohaska, D., and Whitmore, F. C. Jr. 2000. Endocranial volume of mid–late Eocene archaeocetes (Order: Cetacea) revealed by computed tomography: implications of cetacean brain evolution. Journal of Mammalian Evolution 7:8194.Google Scholar
Marino, L., McShea, D. W., and Uhen, M. D. 2004. Origin and evolution of large brains in toothed whales. Anatomical Record Part A 218A:12471255.Google Scholar
Marino, L., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, P. R., Lefebvre, L., Lusseau, D., McCowan, B., Nimchinsky, E. A., Pack, A. A., Rendell, L., Reidenberg, J. S., Reiss, D., Uhen, M. D., van der Gucht, E., and Whitehead, H. 2007. Cetaceans have complex brains for complex cognition. PLoS Biology 5:09660972.Google Scholar
Martin, R. D. 1990. Primate origins and evolution: a phylogenetic reconstruction. Chapman and Hall, London.Google Scholar
Martin, R. D. 1996. Scaling of the mammalian brain: the maternal energy hypothesis. News in Physiological Sciences 11:149156.Google Scholar
Martin, R. D., and McLarnon, A. M. 1985. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313:220223.Google Scholar
Midford, P. E., Garland, T. J., and Maddison, D. R. 2008. PDAP: PDTREE package for Mesquite, Version 1.12. http://mesquiteproject.org/pdap_mesquite/.Google Scholar
Osborne, M. J., Christidis, L., and Norman, J. A. 2002. Molecular phylogenetics of the Diprotodontia (kangaroos, wombats, possums, and allies). Molecular Phylogenetics and Evolution 25:219228.Google Scholar
Pagel, M. D., and Harvey, P. H. 1988. How mammals produce large-brained offspring. Evolution 42:948957.Google Scholar
Pérez-Barberia, F. J., and Gordon, I. J. 2005. Gregariousness increases brain size in ungulates. Oecologia 145:4152.CrossRefGoogle ScholarPubMed
Pérez-Barberia, F. J., Shultz, S., and Dunbar, R. I. M. 2007. Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61:28112821.Google Scholar
Phillips, M. J., Bennett, T. H., and Lee, M. S. Y. 2009. Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proceedings of the National Academy of Sciences USA 106:1708917094.Google Scholar
R Development Core Team. 2009. R: a language and environment for statistical computing, Version 2.7.0. R Foundation for Statistical Computing, Vienna.Google Scholar
Radinsky, L. B. 1969. Outlines of canid and felid brain evolution. Annals of the New York Academy of Sciences 167:277288.Google Scholar
Radinsky, L. B. 1975. Evolution of the felid brain. Brain, Behavior and Evolution 11:214254.Google Scholar
Radinsky, L. B. 1977. Early primate brains: facts and fiction. Journal of Human Evolution 6:7986.CrossRefGoogle Scholar
Radinsky, L. B. 1985. Approaches in evolutionary morphology: a search for patterns. Annual Review of Ecology, Evolution, and Systematics 16:114.Google Scholar
Rowe, T. 1996. Coevolution of the mammalian middle ear and neocortex. Science 273:651653.Google Scholar
Rowe, T., Macrini, T. E., and Luo, Z.-X. 2011. Fossil evidence on the origin of the mammalian brain. Science 332:955957.Google Scholar
Seiffert, E. R. 2007. A new estimate of afrotherian phylogeny based on simultaneous analysis of genomic, morphological, and fossil evidence. BMC Evolutionary Biology 7:224.Google Scholar
Shultz, S., and Dunbar, R. I. M. 2006. Both social and ecological factors predict ungulate brain size. Proceedings of the Royal Society of London B 273:207215.Google ScholarPubMed
Sol, D., Stirling, D. Gray, and Lefebvre, L. 2007. Behavioural drive or behavioural inhibition in evolution: subspecific diversification in holarctic passerines. Evolution 59:2669–2667.Google Scholar
Sol, D., Bacher, S., Reader, S. M., and Lefebvre, L. 2008. Brain size predicts the success of mammal species introduced into novel environments. American Naturalist 172:S63S71.Google Scholar
Steppan, S. J., Storz, B. L., and Homann, R. S. 2004. Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAG1. Molecular Phylogenetics and Evolution 30:703719.Google Scholar
Vaisnys, J., Lieberman, D., and Pilbeam, D. 1984. An alternative method of estimating the cranial capacity of Olduvai Hominid 7. American Journal of Physical Anthropology 65:7181.Google Scholar
Walker, A., Falk, D., Smith, R. and Pickford, M. 1984. The skull of Proconsul africanus: reconstruction and cranial capacity. Nature 305:525527.CrossRefGoogle Scholar
Walker, E. P., and Nowak, R. M., eds. 1999. Walker's mammals of the world. Johns Hopkins University Press, Baltimore.Google Scholar
Weisbecker, V., and Goswami, A. 2010. Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proceedings of the National Academy of Sciences USA 107:1621616221.CrossRefGoogle ScholarPubMed
Wesley-Hunt, G. D. 2005. The morphological diversification of carnivores in North America. Paleobiology 31:3555.Google Scholar
Williams, M. F. 2002. Primate encephalization and intelligence. Medical Hypothesis 58:284290.Google Scholar
Wilson, D., and Reeder, D. M. 2005. Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore.Google Scholar
Wroe, S., and Milne, N. 2007. Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evolution 61:12511260.CrossRefGoogle ScholarPubMed
Zrzavy, J., and Ricanova, V. 2004. Phylogeny of recent Canidae (Mammalia, Carnivora): relative reliability and utility of morphological and molecular datasets. Zoologica Scripta 33:311333.Google Scholar