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Hierarchy and the reconstruction of evolutionary trends: evidence for constraints on the evolution of body size in terrestrial caniform carnivorans (Mammalia)

Published online by Cambridge University Press:  08 April 2016

John A. Finarelli*
Affiliation:
Department of Geological Sciences, University of Michigan, 2534 C. C. Little Building, 1100 North University Avenue, Ann Arbor, Michigan 48109

Abstract

Body mass is an important organism-level variable in mammalian biology, correlated with physiology, life history, and ecology. To analyze the dynamics of body size evolution, increases and decreases in body mass were tallied for ancestor-descendant (AD) species pairs for 519 terrestrial caniform taxa. To account for uncertainty phylogeny, a bootstrapping routine shuffled hypothesized AD pairs, and average proportions of increases were binned as a function of ancestral body mass. A set of models relating the rate of body size increase were evaluated with the Akaike Information Criterion (AIC). AIC selected three models of the candidate set as equivalent in support by the observed body mass data. These three models propose body size increase for small AD pairs and body size decrease for large AD pairs, although they differ in their treatment of taxa at intermediate sizes.

These results demonstrate the presence of constraints bounding the caniform distribution at large and small body sizes, stabilizing the distribution through time, which stands in contrast to a broader mammalian pattern. At a finer phylogenetic scale, subclades within intermediate size classes display proportions that are significantly different from unbiased, with several clades previously cited as examples of “Cope's Rule” showing biased increases in size, and basal mustelids (badgers, and allied genera), Mephitidae (skunks), and Vulpini (“foxes”) exhibiting biased decreases. The caniform pattern is therefore the result of superimposed, clade-specific trajectories, demonstrating that the inferred dynamics of body size evolution and even the direction of trends in body size evolution within the Caniformia, and for mammals in general, depend on the hierarchical scale of the analysis.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Akaike, H. 1973. Information theory as an extension of the maximum likelihood principle. Pp. 267281 in Petrov, B. N. and Csaki, F., eds. Second international symposium on information theory. Akademiai Kiado, Budapest.Google Scholar
Akaike, H. 1974. A new look at the statistical model identification. Institute of Electrical and Electronics Engineers Transactions on Automatic Control AC- 19:716–23.Google Scholar
Alroy, J. 1998. Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science 280:731734.Google Scholar
Alroy, J. 2000. Understanding the dynamics of trends within evolving lineages. Paleobiology 26:319329.Google Scholar
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J. Jr., Sommers, M. G., Wagner, P. J., and Webber, A. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversity. Proceedings of the National Academy of Sciences USA 98:62616266.Google Scholar
Anyonge, W. 1993. Body-mass in large extant and extinct carnivores. Journal of Zoology 231:339350.Google Scholar
Bardeleben, C., Moore, R. L., and Wayne, R. K. 2005. A molecular phylogeny of the Canidae based on six nuclear loci. Molecular Phylogenetics and Evolution 37:815831.Google Scholar
Baskin, J. A. 1989. Comments on New World Tertiary Procyonidae (Mammalia: Carnivora). Journal of Vertebrate Paleontology 9:110117.Google Scholar
Baskin, J. A. 1998a. Mustelidae. Pp. 152173 in Janis, et al. 1998.Google Scholar
Baskin, J. A. 1998b. Procyonidae. Pp. 144151 in Janis, et al. 1998.Google Scholar
Bookstein, F. L., Gingerich, P. D., and Kluge, A. G. 1978. Hierarchical linear modeling of the tempo and mode of evolution. Paleobiology 4:120134.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
Carbone, C., Mace, G. M., Roberts, S. C., and Macdonald, D. W. 1999. Energetic constraints on the diet of terrestrial carnivores. Nature 402:286288.CrossRefGoogle ScholarPubMed
Carbone, C., Teacher, A., and Rowcliffe, J. M. 2007. The cost of carnivory. PLoS Biology 5:03630368.Google Scholar
Edwards, A. W. F. 1992. Likelihood, expanded ed. Johns Hopkins University Press, Baltimore.Google Scholar
Finarelli, J. A. 2007. Mechanisms behind active trends in body size evolution in the Canidae (Carnivora: Mammalia). American Naturalist 170:876885.Google Scholar
Finarelli, J. A. 2008. A total evidence phylogeny of the Arctoidea (Carnivora: Mammalia): relationships among basal taxa. Journal of Mammalian Evolution (published online 01-29-08); DOI: 10.1007/s10914-008-9074-x.Google Scholar
Finarelli, J. A., and Flynn, J. J. 2006. Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record. Systematic Biology 55:301313.Google Scholar
Flynn, J. J., Nedbal, M. A., Dragoo, J. W., and Honeycutt, R. L. 2000. Whence the red panda? Molecular Phylogenetics and Evolution 17:190199.CrossRefGoogle ScholarPubMed
Flynn, J. J., Finarelli, J. A., Zehr, S., Hsu, J., and Nedbal, M. A. 2005. Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Systematic Biology 54:317337.Google Scholar
Friscia, A. R., Van Valkenburgh, B., and Biknevicius, A. R. 2007. An ecomorphological analysis of extant small carnivorans. Journal of Zoology 272:82100.Google Scholar
Fulton, T. L., and Strobeck, C. 2006. Molecular phylogeny of the Arctoidea (Carnivora): effect of missing data on supertree and supermatrix analyses of multiple gene data sets. Molecular Phylogenetics and Evolution 41:165181.Google Scholar
Gingerich, P. D. 1977. Correlation of tooth size and body size in living hominoid primates, with a note on relative brain size in Aegyptopithecus and Proconsul . American Journal of Physical Anthropology 47:395398.CrossRefGoogle ScholarPubMed
Gingerich, P. D. 1990. Prediction of body mass in mammalian species from long bone lengths and diameters. Contributions from the Museum of Paleontology. Museum of Paleontology 28:7992. University of Michigan, Ann Arbor.Google Scholar
Gingerich, P. D., Smith, H. B., and Rosenberg, K. 1982. Allometric scaling in the dentition of Primates and prediction of body weight from tooth size in fossils. American Journal of Physical Anthropology 58:81100.Google Scholar
Gittleman, J. L. 1986. Carnivore life history patterns: allometric, phylogenetic, and ecological associations. American Naturalist 127:744771.Google Scholar
Gittleman, J. L. 1991. Carnivore olfactory bulb size: allometry, phylogeny and ecology. Journal of Zoology 225:253272.Google Scholar
Gittleman, J. L. 1993. Carnivore life histories: a reanalysis in light of new models. Pp. 6586 in Dunstone, N. and Gorman, M., eds. Mammals as predators. Proceedings of a symposium held by the Zoological Society of London and the Mammal Society, London, 22–23 November 1991. Clarendon, New York.CrossRefGoogle Scholar
Gittleman, J. L., and Harvey, P. H. 1982. Carnivore home-range size, metabolic needs and ecology. Behavioral Ecology and Sociobiology 10:5763.Google Scholar
Gittleman, J. L., and Purvis, A. 1998. Body size and species-richness in carnivores and primates. Proceedings of the Royal Society of London B 265–113–119.Google Scholar
Gittleman, J. L., and Van Valkenburgh, B. 1997. Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogeny, and behavioral ecology. Journal of Zoology 242:97117.Google Scholar
Goswami, A. 2006. Morphological integration in the carnivoran skull. Evolution 60:169183.Google Scholar
Gould, S. J. 1988. Trends as changes in variance—a new slant on progress and directionality in evolution. Journal of Paleontology 62:319329.Google Scholar
Hunt, R. M. 1996. Amphicyonidae. Pp. 476485 in Prothero, D. R. and Emry, R. J., eds. The terrestrial Eocene-Oligocene transition in North America. Cambridge University Press, New York.CrossRefGoogle Scholar
Hunt, R. M. 1998a. Amphicyonidae. Pp. 196227 in Janis, et al. 1998.Google Scholar
Hunt, R. M. 1998b. Ursidae. Pp. 174195 in Janis, et al. 1998.Google Scholar
Hurvich, C. M., and Tsai, C.-L. 1989. Regression and time series model selection in small samples. Biometrika 76:297307.Google Scholar
Jablonski, D. 2007. Scale and hierarchy in macroevolution. Palaeontology 50:87109.Google Scholar
Janis, C. M., Scott, K. M., and Jacobs, L. L., eds. 1998. Evolution of Tertiary mammals of North America. Cambridge University Press, New York.Google Scholar
King, C. M. 1989. The advantages and disadvantages of small size to weasels, Mustela species. Pp. 302334 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, N.Y. Google Scholar
Knouft, J. H., and Page, L. M. 2003. The evolution of body size in extant groups of North American freshwater fishes: speciation, size distributions, and Cope's rule. American Naturalist 161:413421.Google Scholar
Legendre, S., and Roth, C. 1988. Correlation of carnassial tooth size and body weight in Recent carnivores (Mammalia). Historical Biology 1:8598.CrossRefGoogle Scholar
McNab, B. K. 1988. Complications inherent in scaling the basal rate of metabolism in mammals. Quarterly Review of Biology 63:2554.Google Scholar
Moen, D. S. 2006. Cope's rule in cryptodiran turtles: do the body sizes of extant species reflect a trend of phyletic size increase? Journal of Evolutionary Biology 19:12101221.Google Scholar
Muñoz-Garcia, A., and Williams, J. B. 2005. Basal metabolic rate in carnivores is associated with diet after controlling for phylogeny. Physiological and Biochemical Zoology 78:10391056.Google Scholar
Novak-Gottshall, P. M., and Lanier, M. A. 2008. Scale-dependence of Cope's rule in body size evolution of Paleozoic brachiopods. Proceedings of the National Academy of Sciences USA 105:54305434.Google Scholar
Royall, R. M. 1997. Statistical evidence: a likelihood paradigm. Chapman and Hall, New York.Google Scholar
Ruff, C. 1990. Body mass and hindlimb bone cross-sectional and articular dimensions in anthropoid Primates. Pp. 119149 in Damuth, J. and MacFadden, B. J., eds. Body size in mammalian paleobiology. Cambridge University Press, New York.Google Scholar
Sato, J. J., Hosoda, T., Wolsan, M., Tsuchiya, K., Yamamo, M., and Suzuki, H. 2003. Phylogenetic relationships and divergence times among mustelids (Mammalia: Carnivora) based on nucleotide sequences of the nuclear interphotoreceptor retinoid binding protein and mitochondrial cytochrome b genes. Zoological Science 20:243264.Google Scholar
Sato, J. J., Hosoda, T., Wolsan, M., and Suzuki, H. 2004. Molecular phylogeny of arctoids (Mammalia: Carnivora) with emphasis on phylogenetic and taxonomic positions of the ferret-badgers and skunks. Zoological Science 21:111118.Google Scholar
Sato, J. J., Wolsan, M., Suzuki, H., Hosoda, T., Yamaguchi, Y., Hiyama, K., Kobayashi, M., and Minami, S. 2006. Evidence from nuclear DNA sequences sheds light on the phylogenetic relationships of Pinnipedia: single origin with affinity to Musteloidea. Zoological Science 23:125146.Google Scholar
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge University Press, Cambridge.Google Scholar
Sears, K. E., Finarelli, J. A., Flynn, J. J., and Wyss, A. R. 2008. Estimating body mass in New World “monkeys” (Platyrrhini, Primates) from craniodental measurements, with a consideration of the Miocene platyrrhine, Chilecebus carrascoensis . American Museum Novitates 3617:129.CrossRefGoogle Scholar
Stanley, S. M. 1973. An explanation for Cope's rule. Evolution 27:126.Google Scholar
Van Valkenburgh, B. 1989. Carnivore dental adaptations and diet: a study of trophic diversity within guilds. Pp. 410436 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, N.Y. Google Scholar
Van Valkenburgh, B. 1990. Skeletal and dental predictors of body mass in carnivores. Pp. 181206 in Damuth, J. and MacFadden, B. J., eds. Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, New York.Google Scholar
Van Valkenburgh, B. 1991. Iterative evolution of hypercarnivory in canids (Mammalia, Carnivora): evolutionary interactions among sympatric predators. Paleobiology 17:340362.Google Scholar
Van Valkenburgh, B. 1999. Major patterns in the history of carnivorous mammals. Annual Review of Earth and Planetary Sciences 27:463493.Google Scholar
Van Valkenburgh, B., Sacco, T., and Wang, X. M. 2003. Pack hunting in Miocene borophagine dogs: evidence from craniodental morphology and body size. Bulletin of the American Museum of Natural History 279:147162.Google Scholar
Van Valkenburgh, B., Wang, X. M., and Damuth, J. 2004. Cope's Rule, hypercarnivory, and extinction in North American canids. Science 306:101104.CrossRefGoogle ScholarPubMed
Wagner, P. J. 2000. Phylogenetic analyses and the fossil record: tests 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
Wang, X. M. 1994. Phylogenetic systematics of the Hesperocyoninae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 221:1207.Google Scholar
Wang, X. M., Tedford, R. H., and Taylor, B. E. 1999. Phylogenetic systematics of the Borophaginae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 243:1391.Google Scholar
Wang, X. M., McKenna, M., and Dashzeveg, D. 2005a. Amphicticeps and Amphicynodon (Arctoidea, Carnivora) from Hsanda Gol Formation, central Mongolia and phylogeny of basal arctoids with comments on zoogeography. American Museum Novitates 3483:157.Google Scholar
Wang, X. M., Whistler, D. P., and Takeuchi, G. T. 2005b. A new basal skunk Martinogale (Carnivora, Mephitinae) from late Miocene Dove Spring Formation, California, and origin of New World mephitines. Journal of Vertebrate Paleontology 25:936949.Google Scholar
Webster, A. J., Gittleman, J. L., and Purvis, A. 2004. The life history legacy of evolutionary body size change in carnivores. Journal of Evolutionary Biology 17:396407.Google Scholar
Wesley-Hunt, G. D., and Flynn, J. J. 2005. Phylogeny of the Carnivora: basal relationships among the carnivoramorphans, and assessment of the position of “Miacoidea” relative to crown-clade Carnivora. Journal of Systematic Palaeontology 3:128.Google Scholar
Wilson, E. B. 1927. Probable inference, the law of succession, and statistical inference. Journal of the American Statistical Association 22:209212.Google Scholar
Yu, L., Li, Q., Ryder, O. A., and Zhang, Y. 2004. Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution 32:480494.Google Scholar
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