Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T19:19:05.710Z Has data issue: false hasContentIssue false

Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity

Published online by Cambridge University Press:  08 April 2016

Jill A. Holliday
Affiliation:
Department of Biological Science, Florida State University, Tallahassee, Florida 32306–1100. E-mail: [email protected], [email protected]
Scott J. Steppan
Affiliation:
Department of Biological Science, Florida State University, Tallahassee, Florida 32306–1100. E-mail: [email protected], [email protected]

Abstract

The effects of specialization on subsequent morphological evolution are poorly understood. Specialization has been implicated in both adaptive radiations that result from key innovations and evolutionary “dead ends,” where specialized characteristics appear to limit subsequent evolutionary options. Despite much theoretical debate, however, empirical studies remain infrequent. In this paper, we use sister-group comparisons to evaluate the effect of morphological specialization to a particular ecological niche, hypercarnivory, on subsequent taxonomic and morphological diversity. Six sets of sister groups are identified in which one clade exhibits hypercarnivorous characteristics and the sister clade does not. Comparison results are summed across the categories “hypercarnivore” and “sister group.” We also evaluate whether increasing degrees of specialization are correlated with decreasing phenotypic variation. Results presented here indicate that specialization to hypercarnivory has no effect on taxonomic diversity, but a strong effect on subsequent morphological diversity related to the jaws and dentition, and that increasing specialization does not correlate with morphological diversity except in the most specialized sabertoothed taxa, which exhibit higher variance than less specialized morphs, possibly due to selection on other characteristics.

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

Baskin, J. A. 1981. Barbourofelis (Nimravidae) and Nimravides (Felidae) with a description of two new species from the late Miocene of Florida. Journal of Mammalogy 62:122139.Google Scholar
Baskin, J. A. 1998. Mustelidae. Pp. 152173in Janis, et al. 1998.Google Scholar
Berta, A. 1987. The sabercat Smilodon gracilis from Florida and a discussion of its relationships (Mammalia, Felidae, Smilodontini). Bulletin of the American Museum of Natural History 31:163.Google Scholar
Berta, A. 1998. Hyaenidae. Pp. 243246in Janis, et al. 1998.Google Scholar
Berta, A., and Galiano, H. 1983. Megantereon hesperus from the late Hemphillian of Florida with remarks on the phylogenetic relationships of machairodonts (Mammalia, Felidae, Machairodontinae). Journal of Paleontology 57: 892–800.Google Scholar
Biknevicius, A. R., and Van Valkenburgh, B. 1996. Design for killing: craniodental adaptations of predators. Pp. 393428in Gittleman, 1996.Google Scholar
Bininda-Emonds, O. R. P., Gittleman, J. L., and Purvis, A. 1999. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biological Reviews of the Cambridge Philosophical Society 74:143175.Google Scholar
Brooks, D. R., and McLennan, D. A. 1991. Phylogeny, ecology and behavior. University of Chicago Press, Chicago.Google Scholar
Bryant, H. N. 1991. Phylogenetic relationships and systematics of the Nimravidae (Carnivora). Journal of Mammalogy 72:5678.Google Scholar
Bryant, H. N. 1996. Nimravidae. Pp. 453475in Prothero, D. R. and Emry, R. J., eds. The terrestrial Eocene–Oligocene transition in North America. Cambridge University Press, Cambridge.Google Scholar
Bryant, H. N., Russell, A. P., and Fitch, W. D. 1993. Phylogenetic relationships within the extant Mustelidae (Carnivora)—appraisal of the cladistic status of the Simpsonian subfamilies. Zoological Journal of the Linnean Society 108:301334.Google Scholar
Crusafont-Pairo, M., and Truyols-Santonja, J. 1956. A biometric study of the evolution of fissiped carnivores. Evolution 10:314332.Google Scholar
Dayan, T., Simberloff, D., Tchernov, E., and Yom-Tov, Y. 1989. Inter- and intraspecific character displacement in mustelids. Ecology 70:15261539.Google Scholar
Dayan, T. 1990. Feline canines: community-wide character displacement among the small cats of Israel. American Naturalist 136:3960.Google Scholar
de Queiroz, A. 1998. Interpreting sister group tests of key innovation hypotheses. Systematic Biology 47:710718.Google Scholar
de Queiroz, A. 1999. Do image-forming eyes promote evolutionary diversification? Evolution 53:16541664.Google Scholar
Dillon, W. R., and Goldstein, M. 1984. Multivariate analysis. Wiley, New York.Google Scholar
Dodd, M. E., Silvertown, J., and Chase, M. W. 1999. Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53:732744.Google Scholar
Donoghue, M. J., and Ree, R. H. 2000. Homoplasy and developmental constraint: a model and an example from plants. American Zoologist 40:759769.Google Scholar
Dragoo, J. W., and Honeycutt, R. L. 1997. Systematics of mustelid-like carnivores. Journal of Mammalogy 78:426443.Google Scholar
Eble, G. J. 2000. Contrasting evolutionary flexibility in sister groups: disparity and diversity in Mesozoic atelostomate echinoids. Paleobiology 26:5679.Google Scholar
Emerson, S. B. 1988. Testing for historical patterns of change—a case-study with frog pectoral girdles. Paleobiology 14:174186.Google Scholar
Estes, J. A. 1989. Adaptations for aquatic living by carnivores. Pp. 242282in Gittleman, 1989.Google Scholar
Ewer, R. F. 1973. The carnivores. Cornell University Press, Ithaca, N.Y.Google Scholar
Farrell, B. D., Dussourd, D. E., and Mitter, C. 1991. Escalation of plant defense—do latex and resin canals spur plant diversification. American Naturalist 138:881900.Google Scholar
Flynn, J. J., and Nedbal, M. A. 1998. Phylogeny of the Carnivora (Mammalia): congruence vs. incompatibility among multiple data sets. Molecular Phylogenetics and Evolution 9:414426.Google Scholar
Flynn, J. J., Neff, N. A., and Tedford, R. H. 1988. Phylogeny of the Carnivora. Pp. 73116in Benton, M. J., ed. The phylogeny and classification of the tetrapods. Clarendon, Oxford.Google Scholar
Foote, M. 1992. Rarefaction analysis of morphological and taxonomic diversity. Paleobiology 18:116.Google Scholar
Foote, M. 1993. Discordance and concordance between morphological and taxonomic diversity. Paleobiology 19:185204.Google Scholar
Foote, M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics 28:129152.Google Scholar
Futuyma, D. J., and Moreno, G. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207233.Google Scholar
Gardezi, T., and da Silva, J. 1999. Diversity in relation to body size in mammals: a comparative study. American Naturalist 153:110123.Google Scholar
Geraads, D., and Gulec, E. 1997. Relationships of Barbourofelis piveteaui (Ozansoy, 1965), a late Miocene nimravid (Carnivora, Mammalia) from central Turkey. Journal of Vertebrate Paleontology 17:370375.Google Scholar
Gingerich, P. D. 1974. Size variability in living mammals and diagnosis of closely related sympatric fossil species. Journal of Paleontology 48:895903.Google Scholar
Ginsberg, L. 1983. Sur les modalités d'évolution du genre Neogene Pseudaelurus Gervais (Felidae, Carnivora, Mammalia). Colloques Internationaux du CNRS 330:131136.Google Scholar
Gittleman, J. L., ed. 1989. Carnivore behavior, ecology and evolution, Vol. I. Cornell University Press, Ithaca, N.Y.Google Scholar
Gittleman, J. L., ed. 1996. Carnivore behavior, ecology and evolution, Vol. II. Cornell University Press, Ithaca, N.Y.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 265:113119.Google Scholar
Glass, G. E., and Martin, L. D. 1978. Multivariate comparison of some extant and fossil Felidae. Carnivore 1:8087.Google Scholar
Hemmer, H. 1978. Fossil history of living Felidae. Carnivore 2:5861.Google Scholar
Hodges, S. A., and Arnold, M. L. 1995. Spurring plant diversification: are floral nectar spurs a key innovation? Proceedings of the Royal Society of London B 262:343348.Google Scholar
Hunt, R. M. Jr. 1987. Evolution of the aeluroid Carnivora: significance of auditory structure in the nimravid cat Dinictis. American Museum Novitates 2886:174.Google Scholar
Hunt, R. M. Jr. 1996. Biogeography of the order Carnivora. Pp. 485541in Gittleman, 1996.Google Scholar
Hunt, R. M. Jr. 1998. Evolution of the aeluroid Carnivora: diversity of the earliest aeluroids from Eurasia (Quercy, Hsanda-Gol) and the origin of felids. American Museum Novitates 3252:165.Google Scholar
Hunt, R. M. Jr., and Tedford, R. H. 1993. Phylogenetic relationships within the aeluroid Carnivora and implications of their temporal and geographic distribution. Pp. 5373in Szalay, F. S., Novacek, J. J., and McKenna, M. C., eds. Mammal phylogeny. Springer, New York.Google Scholar
Janis, C. M., Scott, K. M., and Jacobs, L. L., eds. 1998. Evolution of Tertiary mammals of North America. Cambridge University Press, Cambridge.Google Scholar
Janz, N., Nyblom, K., and Nylin, S. 2001. Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini. Evolution 55:783796.Google Scholar
Kieser, J. A., and Groeneveld, H. 1991. Fluctuating odontometric asymmetry, morphological variability and genetic monomorphism in the cheetah Acinonyx jubatus. Evolution 45:11751183.Google Scholar
King, C. 1989. The advantages and disadvantages of small size to weasels, Mustela species. Pp. 302334in Gittleman, 1989.Google Scholar
Koepfli, K. P., and Wayne, R. K. 1998. Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial cytochrome b sequences. Journal of Zoology 246:401416.Google Scholar
Koepfli, K. P., and Wayne, R. K. 2003. Type-I STS markers are more informative than cytochrome b in phylogenetic estimation of the Mustelidae (Mammalia: Carnivora). Systematic Biology (in press).Google Scholar
Lauder, G. V. 1981. Form and function—structural-analysis in evolutionary morphology. Paleobiology 7:430442.Google Scholar
Liem, K. 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22:425441.Google Scholar
Martin, L. D. 1980. Functional morphology and the evolution of cats. Transactions of the Nebraska Academy of Sciences 8:141154.Google Scholar
Martin, L. D. 1989. Fossil history of the terrestrial Carnivora. Pp. 536568in Gittleman, 1989.Google Scholar
Martin, L. D. 1998a. Felidae. Pp. 236242in Janis, et al. 1998.Google Scholar
Martin, L. D. 1998b. Nimravidae. Pp. 228235in Janis, et al. 1998.Google Scholar
Masuda, R., and Yoshida, M. C. 1994. A molecular phylogeny of the family Mustelidae (Mammalia, Carnivora), based on comparison of mitochondrial cytochrome b nucleotide sequences. Zoological Science 11:605612.Google Scholar
Mattern, M. Y., and McLennan, D. A. 2000. Phylogeny and speciation of felids. Cladistics 16:232253.Google Scholar
McShea, D. W. 2001. The minor transitions in hierarchical evolution and the question of a directional bias. Journal of Evolutionary Biology 14:502518.Google Scholar
Mitter, C., Farrell, B., and Wiegmann, B. 1988. The phylogenetic study of adaptive zones—has phytophagy promoted insect diversification? American Naturalist 132:107128.Google Scholar
Morales, J., Salesa, M. J., Pickford, M., and Soria, D. 2001. A new tribe, new genus and two new species of Barbourofelinae (Felidae, Carnivora, Mammalia) from the early Miocene of East Africa and Spain. Transactions of the Royal Society of Edinburgh (Earth Sciences) 92:97102.Google Scholar
Morlo, M. S., Peigné, S., and Nagel, D. 2003. A new species of Prosansanosmilus: implications for the systematic relationships of the family Barbourofelidae new rank (Carnivora: Mammalia). Zoological Journal of the Linnean Society (in press).Google Scholar
Moran, N. A. 1988. The evolution of host-plant alternation in aphids—evidence for specialization as a dead end. American Naturalist 132:681706.Google Scholar
Nee, S., Holmes, E. C., Rambaut, A., and Harvey, P. H. 1995. Inferring population history from molecular phylogenies. Philosophical Transactions of the Royal Society of London B 344:2531.Google Scholar
Neff, N. 1982. The big cats. Harry N. Abrams, New York.Google Scholar
Neff, N. 1983. The basicranial anatomy of the Nimravidae (Mammalia: Carnivora): character analyses and phylogenetic inferences. . City University, New York.Google Scholar
Nowak, R. M. 1999. Walker's mammals of the world. Johns Hopkins University Press, Baltimore.Google Scholar
O'Regan, H. J. 2002. Defining cheetahs, a multivariate analysis of skull shape in big cats. Mammal Review 32:5862.Google Scholar
Price, P. W., and Carr, T. G. 2000. Comparative ecology of membracids and tenthredinids in a macroevolutionary context. Evolutionary Ecology Research 2:645665.Google Scholar
Radinsky, L. B. 1981a. Evolution of skull shape in carnivores. 1. Representative modern carnivores. Biological Journal of the Linnean Society 15:369388.Google Scholar
Radinsky, L. B. 1981b. Evolution of skull shape in carnivores. 2. Additional modern carnivores. Biological Journal of the Linnean Society 16:337355.Google Scholar
Radinsky, L. B. 1982. Evolution of skull shape in carnivores. 3. The origin and early radiation of the modern carnivore families. Paleobiology 8:177195.Google Scholar
Roy, K., and Foote, M. 1997. Morphological approaches to measuring biodiversity. Trends in Ecology and Evolution 12:277281.Google Scholar
Russell, A. P., Bryant, H. N., Powell, G. L., and Laroiya, R. 1995. Scaling relationships within the maxillary tooth row of the Felidae, and the absence of the 2nd upper premolar in Lynx. Journal of Zoology 236:161182.Google Scholar
Sanderson, M. J. 1993. Reversibility in evolution—a maximum-likelihood approach to character gain loss bias in phylogenies. Evolution 47:236252.Google Scholar
Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.Google Scholar
Slowinski, J. B., and Guyer, C. 1993. Testing whether certain traits have caused amplified diversification—an improved method based on a model of random speciation and extinction. American Naturalist 142:10191024.Google Scholar
Smith, J. F. 2001. High species diversity in fleshy-fruited tropical understory plants. American Naturalist 157:646653.Google Scholar
Smith, J. M., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., and Wolpert, L. 1985. Developmental constraints and evolution. Quarterly Review of Biology 60:265287.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1994. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Turner, A., and Anton, M. 1997. The big cats and their fossil relatives. Columbia University Press, New York.Google Scholar
Van Valkenburgh, B. 1988. Trophic diversity in past and present guilds of large predatory mammals. Paleobiology 14:155173.Google Scholar
Van Valkenburgh, B. 1989. Carnivore dental adaptations and diet: a study of trophic diversity within guilds. Pp. 410436in Gittleman, 1989.Google Scholar
Van Valkenburgh, B. 1990. Skeletal and dental predictors of body mass in carnivores. Pp. 181205in Damuth, J. and MacFadden, B. J., eds. Body size in mammalian paleobiology: estimation and biological implications. Cambridge University Press, Cambridge.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., and Ruff, C. B. 1987. Canine tooth strength and killing behavior in large carnivores. Journal of Zoology 212:379397.Google Scholar
Veron, G. 1995. La position systématique de Cryptoprocta ferox (Carnivora). Analyse cladistique des caractères morphologiques de carnivores Aeluroidea actuels et fossiles. Mammalia 59:551582.Google Scholar
Veron, G., and Catzeflis, F. M. 1993. Phylogenetic relationships of the endemic Malagasy carnivore Cryptoprocta ferox (Aeluroidea): DNA/DNA hybridization experiments. Journal of Mammalian Evolution 1:169185.Google Scholar
Veron, G., and Heard, S. 1999. Molecular systematics of the Asiatic Viverridae (Carnivora) inferred from mitochondrial cytochrome b sequence analysis. Journal of Zoological Systematics and Evolutionary Research 38:209217.Google Scholar
Wagner, G. P., and Schwenk, K. 2000. Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. Pp. 155217in Hecht, M. K., ed. Evolutionary biology. Plenum, New York.Google Scholar
Wang, X. 1994. Phylogenetic systematics of the Hesperocyoninae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 221:1207.Google Scholar
Wang, X., 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
Warheit, K. I., Forman, J. D., Losos, J. B., and Miles, D. B. 1999. Morphological diversification and adaptive radiation: a comparison of two diverse lizard clades. Evolution 53:12261234.Google Scholar
Werdelin, L. 1983. Morphological patterns in the skulls of cats. Biological Journal of the Linnean Society 19:375: 391.Google Scholar
Werdelin, L. 1985. Small Pleistocene felines of North America. Journal of Vertebrate Paleontology 5:194210.Google Scholar
Werdelin, L. 1987. Supernumerary teeth in Lynx lynx and the irreversibility of evolution. Journal of Zoology 211:259266.Google Scholar
Werdelin, L. 1989. Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387401.Google Scholar
Werdelin, L. 1996. Carnivoran ecomorphology: a phylogenetic perspective. Pp. 582624in Gittleman, 1996.Google Scholar
Werdelin, L., and Solounias, N. 1991. The Hyaenidae: taxonomy, systematics and evolution. Lethaia 30:1105.Google Scholar
Werdelin, L., and Solounias, N. 1996. The evolutionary history of hyenas in Europe and Western Asia during the Miocene. Pp. 290306in Bernor, R. L., Fahlbusch, V., and Mittmann, H., eds. The evolution of the western Eurasian Neogene mammal faunas. Columbia University Press, New York.Google Scholar
Wiegmann, B. M., Mitter, C., and Farrell, B. 1993. Diversification of carnivorous parasitic insects—extraordinary radiation or specialized dead-end? American Naturalist 142:737754.Google 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 20:93130.Google Scholar
Wozencraft, W. C. 1984. A phylogenetic reappraisal of the Viverridae and its relationship to other Carnivora. . University of Kansas, Lawrence.Google Scholar
Wozencraft, W. C. 1989. The phylogeny of the Recent Carnivora. Pp. 495535in Gittleman, 1989.Google Scholar
Wyss, A. R., and Flynn, J. J. 1993. A phylogenetic analysis and definition of the Carnivora. Pp. 3352in Szalay, F. S., Novacek, J. J., and McKenna, M. C., eds. Mammal phylogeny: placental. Springer, New York.Google Scholar