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Evolution of hypsodonty in equids: testing a hypothesis of adaptation

Published online by Cambridge University Press:  08 April 2016

Caroline A. E. Strömberg
Caroline A. E. Strömberg*
Affiliation:
Departments of Palaeobotany and Palaeozoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden. E-mail: [email protected]
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Abstract

The independent acquisition of high-crowned cheek teeth (hypsodonty) in several ungulate lineages (e.g., camels, equids, rhinoceroses) in the early to middle Miocene of North America has classically been used as an indication that savanna vegetation spread during this time. Implicit in this interpretation is the untested assumption that hypsodonty was an evolutionary response to feeding in open habitats, either due to a change in food source (from browse to graze) or to increased incorporation of airborne grit in the diet. I examined the adaptive explanation for hypsodonty in equids using criteria pertaining to process and pattern of adaptations set up in the comparative-methods literature. Specifically, I tested whether hypsodonty appeared coincident with or just after the spread of open, grass-dominated habitats in the Great Plains of North America.

Phytolith (plant opal) analysis of 99 phytolith assemblages extracted from sediment samples from Montana/Idaho, Nebraska/Wyoming, and Colorado were used to establish the first continuous record of middle Eocene-late Miocene vegetation change in the northern to Central Great Plains. This record was compared with the fossil record of equids from the same area in a phylogenetic framework.

The study showed that habitats dominated by C3 grasses were established in the Central Great Plains by early late Arikareean (≥21.9 Ma), at least 4 Myr prior to the emergence of hypsodont equids (Equinae). Nevertheless, the adaptive hypothesis for hypsodonty in equids could not be rejected, because the earliest savanna-woodlands roughly co-occurred with members of the grade constituting the closest outgroups to Equinae (“Parahippus”) showing mesodont dentition. Explanations for the slow evolution of full hypsodonty may include weak and changing selection pressures and/or phylogenetic inertia. These results suggest that care should be taken when using functional morphology alone to reconstruct habitat change.

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Articles
Information
Paleobiology , Volume 32 , Issue 2 , Spring 2006 , pp. 236 - 258
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Copyright © The Paleontological Society 

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References

Literature Cited

Alroy, J. 1992. Conjunction among taxonomic distributions and the Miocene mammalian biochronology of the Great Plains. Paleobiology 18:326–343.Google Scholar
Alroy, J. 1998. Diachrony of mammalian appearance events: implications for biochronology. Geology 26:23–26.2.3.CO;2>CrossRefGoogle Scholar
Arnold, S. J. 1983. Morphology, performance and fitness. American Zoologist 23:347–361.Google Scholar
Arnold, S. J. 1994. Investigating the origins of perfomance advantage: adaptation, exaptation and lineage effects. Pp. 123–168 in Eggleton, P. and Vane-Wright, R., eds. Phylogenetics and ecology. Academic Press, London.Google Scholar
Arnold, S. J., and Wade, M. J. 1984a. On the measurement of selection in natural and laboratory populations: theory. Evolution 38:709–719.Google Scholar
Arnold, S. J., and Wade, M. J. 1984b. On the measurement of selection in natural and laboratory populations: application. Evolution 38:720–733.CrossRefGoogle Scholar
Bader, R. S. 1956. A quantitative study of the Equidae of the Thomas Farm Miocene. Bulletin of the Museum of Comparative Zoology 115:47–78.Google Scholar
Bailey, B. E. 2004. Biostratigraphy and biochronology of early Arikareean through late Hemingfordian small mammal faunas from the Nebraska panhandle and adjacent areas. Paludicola 4:81–113.Google Scholar
Baker, G., Jones, L. H. P., and Wardrop, I. D. 1959. Cause of wear in sheeps' teeth. Nature 184:1583–1584.Google Scholar
Barreto, G. P., Lira, M. d. A., Santos, M. V. F. d., and Dubeux, J. C. B. Júnior. 2001. Evaluation of elephant grass clones (Pennisetum purpureum Schum.) and an elephant grass X pearl millet (Pennisetum glaucum (L.) R. Br.) hybrid submitted to water stress. 2. Nutritive value. Revista Brasileira de Zootecnia 30:7–11.Google Scholar
Baum, D. A., and Larson, A. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Systematic Biology 40:1–18.CrossRefGoogle Scholar
Bérubé, C., Festa-Bianchet, M., and Jorgenson, J. T. 1999. Individual differences, longevity, and reproductive senescence in bighorn ewes. Ecology 80:2555–2565.Google Scholar
Blackburn, D. G. 2002. Use of phylogenetic analysis to distinguish adaptation from exaptation. Behavioral and Brain Sciences 25:507–508.CrossRefGoogle Scholar
Blomberg, S. P., and Garland, T. J. 2002. Tempo and mode in evolution: phylogenetic intertia, adaptation and comparative methods. Journal of Evolutionary Biology 15:899–910.CrossRefGoogle Scholar
Brandon, R. N. 1990. Adaptation and environment. Princeton University Press, Princeton, N.J. Google Scholar
Brooks, D. R., and McLennan, D. A. 1991. Phylogeny, ecology, and behavior: a research program in comparative biology. University of Chicago Press, Chicago.Google Scholar
Burian, R. M. 1992. Adaptation: historical perspectives. Pp. 7–12 in Keller, E. F. and Lloyd, E. A., eds. Keywords in evolutionary biology. Harvard University Press, Cambridge.Google Scholar
Butler, P. M. 1983. Evolution and mammalian dental morphology. Journal de Biologie Buccale 11:285–302.Google ScholarPubMed
Carpenter, J. M. 1989. Testing scenarios: wasp social behavior. Cladistics 5:131–144.CrossRefGoogle ScholarPubMed
Cid, M. S., Detling, J. K., Brizuela, M. A., and Whicker, A. D. 1989. Patterns in grass silicification: response to grazing history and defoliation. Oecologia 80:268–271.CrossRefGoogle ScholarPubMed
Clutton-Brock, T. H., Albon, S. D., and Guinness, F. E. 1988. Reproductive success in male and female red deer. Pp. 325–343 in Clutton-Brock, T. H., ed. Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago.Google Scholar
Coddington, J. A. 1988. Cladistic tests of adaptational hypotheses. Cladistics 4:3–22.Google Scholar
Coddington, J. A. 1990. Bridges between evolutionary pattern and process. Cladistics 6:379–386.CrossRefGoogle ScholarPubMed
Coddington, J. A. 1994. The roles of homology and convergence in studies of adaptation. Pp. 53–78 in Eggleton, P. and Vane-Wright, R. I., eds. Phylogenetics and ecology. Academic Press, London.Google Scholar
Covert, H. H., and Kay, R. F. 1981. Dental microwear and diet: implications for determining the feeding behaviors of extinct primates, with a comment on the dietary pattern of Sivapithecus . American Journal of Physical Anthropology 55:331–336.CrossRefGoogle ScholarPubMed
Cunningham, C. W., Omland, K. E., and Oakley, T. H. 1998. Reconstructing ancestral character states: a critical reappraisal. Trends in Ecology and Evolution 13:361–366.CrossRefGoogle Scholar
Damuth, J., and Fortelius, M. 2001. Reconstructing mean annual precipitation, based on mammalian dental morphology and local species richness. Pp. 23–24 in Agustí, J. and Oms, O., eds. EEDEN programme plenary workshop on Late Miocene to Early Pliocene environments and ecosystems. European Science Foundation.Google Scholar
de Pinna, M. C. C., and Salles, L. O. 1990. Cladistic tests of adaptational hypotheses: a reply to Coddington. Cladistics 6:373–377.Google Scholar
de Queiroz, K. 2000. Logical problems associated with including and excluding characters during tree reconstruction and their implications for the study of morphological character evolution. Pp. 192–212 in Wiens, J. J., ed. Phylogenetic analysis of morphological data. Smithsonian Institution Press, Washington, D.C. Google Scholar
Downs, T. 1961. A study of variation and evolution in Miocene Merychippus . Los Angeles County Museum, Contributions in Science 45:3–75.Google Scholar
Edwards, S. V., and Naeem, S. 1993. The phylogenetic component of cooperative breeding in perching birds. American Naturalist 141:754–789.Google Scholar
Evander, R. L. 1989. Phylogeny of the family Equidae. Pp. 109–127 in Prothero, and Schoch, 1989.Google Scholar
Feranec, R. S. 2004. Geographic variation in the diet of hypsodont herbivores from the Rancholabrean of Florida. Palaeogeography, Palaeoclimatology, Palaeoecology 207:359–369.CrossRefGoogle Scholar
Forstén, A.-M. 1970a. The late Miocene Trail Creek mammalian fauna. Contributions to Geology 9:39–51.Google Scholar
Forstén, A.-M. 1970b. Variation in and between three populations of Mesohippus bairdii Leidy from the Big Badlands, South Dakota. Acta Zoologica Fennica 126:1–16.Google Scholar
Fortelius, M. 1985. Ungulate cheek teeth: developmental, functional and evolutionary interrelations. Acta Zoologica Fennica 180:1–76.Google Scholar
Fortelius, M., and Solounias, N. 2000. Functional characterization of ungulate molars using the abrasion-attrition wear gradient: a new method for reconstructing paleodiets. American Museum Novitates 3301:1–35.Google Scholar
Fortelius, M., Werdelin, L., Andrews, P., Bernor, R. L., Gentry, A., Humphrey, L., Mittmann, H.-W., and Viratana, S. 1996. Provinciality, diversity, turnover, and paleoecology in land mammal faunas of the later Miocene of western Eurasia. Pp. 414–448 in Bernor, R. L., Fahlbusch, V., and Mittmann, H.-W., eds. The evolution of western Eurasian Neogene mammal faunas. Columbia University Press, New York.Google Scholar
Fortelius, M., Eronen, J. T., Jernvall, J., Liu, L., Pushkina, D., Rinne, J., Tesakov, A., Vislobokova, I. A., Zhang, Z., and Zhou, L. 2002. Fossil mammals resolve regional patterns of Eurasian climate change during 20 million years. Evolutionary Ecology Research 4:1005–1016.Google Scholar
Frumhoff, P. C., and Reeve, H. K. 1994. Using phylogenies to test hypotheses of adaptation: a critique of some current proposals. Evolution 48:172–180.Google Scholar
Gaillard, J.-M., Festa-Bianchet, M., Yoccoz, N. G., Loison, A., and Toïgo, C. 2000a. Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics 31:367–393.Google Scholar
Gaillard, J.-M., Festa-Bianchet, M., Delorme, D., and Jorgenson, J. T. 2000b. Body mass and reproductive success in female ungulates: bigger is not always better! Proceedings of the Royal Society of London B 267:471–477.Google Scholar
Garrott, R. A., Eagle, T. C., and Plotka, E. D. 1991. Age-specific reproduction in feral horses. Canadian Journal of Zoology 69:738–743.CrossRefGoogle Scholar
Gingerich, P. D. 1981. Variation, sexual dimorphism, and social structure in the early Eocene horse Hyracotherium (Mammalia, Perissodactyla). Paleobiology 7:443–455.Google Scholar
Gould, S. J. 2002. The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Gould, S. J., and Vrba, E. S. 1982. Exaptation—a missing term in the science of form. Paleobiology 8:4–15.CrossRefGoogle Scholar
Grandcolas, P., and D'Haese, C. 2003. Testing adaptation with phylogeny: how to account for phylogenetic pattern and selective value together. Zoologica Scripta 32:483–490.CrossRefGoogle Scholar
Greene, H. W. 1986. Diet and arboreality in the emerald monitor, Varanus prasinus, with comments on the study of adaptation. Fieldiana (Zoology) 31:1–12.Google Scholar
Groot, J. C. J., Lantinga, E. A., Neuteboom, J. H., and Deinum, B. 2003. Analysis of the temperature effect on the components of plant digestibility in two populations of perennial ryegrass. Journal of the Science of Food and Agriculture 83:320–329.Google Scholar
Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341–1351.Google Scholar
Harvey, P. H., and Pagel, M. D. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford.Google Scholar
Hayek, L. A. C., Bernor, R. L., Solounias, N., and Steigerwald, P. 1992. Preliminary studies of hipparionine horse diet as measured by tooth microwear. Pp. 187–200 in Forstén, A., Fortelius, M., and Werdelin, L., eds. Björn Kurtén–a memorial volume.Google Scholar
Henry, D. A., Simpson, R. J., and Macmillan, R. H. 2000. Seasonal changes and the effect of temperature and leaf moisture content on intrinsic shear strength of leaves of pasture grasses. Australian Journal of Agricultural Research 51:823–831.Google Scholar
Hiiemae, K. M. 2000. Feeding in mammals. Pp. 411–448 in Schwenk, K., ed. Feeding: form, function, and evolution in tetrapod vertebrates. Academic Press, San Diego.CrossRefGoogle Scholar
Hooker, J. J. 1989. Character polarities in early perissodactyls and their significance for Hyracotherium and infraordinal relationships. Pp. 79–108 in Prothero, and Schoch, 1989.Google Scholar
Hopkins, S. S. B. 2005. The evolution of fossoriality and the adaptive role of horns in the Mylagaulidae (Mammalia: Rodentia). Proceedings of the Royal Society of London B 272:1705–1713.Google Scholar
Hulbert, R. C. Jr. 1982. Population dynamics of the three-toed horse Neohipparion from the late Miocene of Florida. Paleobiology 8:159–167.Google Scholar
Hulbert, R. C. Jr. 1984. Paleoecology and population dynamics of the early Miocene (Hemingfordian) horse Parahippus leonensis from the Thomas Farm site, Florida. Journal of Vertebrate Paleontology 4:547–558.Google Scholar
Hulbert, R. C. Jr. 1989. Phylogenetic interrelationships and evolution of North American late Neogene Equinae. Pp. 176–196 in Prothero, and Schoch, 1989.Google Scholar
Hulbert, R. C. Jr., and MacFadden, B. J. 1991. Morphological transformation and cladogenesis at the base of the adaptive radiation of Miocene hypsodont horses. American Museum Novitates 3000:1–61.Google Scholar
Huxley, J. 1953. Evolution in action. Chatto and Windus, London.Google Scholar
Jacobs, B. F., Kingston, J. D., and Jacobs, L. L. 1999. The origin of grass-dominated ecosystems. Annals of the Missouri Botanical Garden 86:590–643.Google Scholar
Janis, C. M. 1982. Evolution of horns in ungulates: ecology and paleoecology. Biological Reviews of the Cambridge Philosophical Society 57:261–318.Google Scholar
Janis, C. M. 1984. The use of fossil ungulate communities as indicators of climate and environment. Pp. 85–104 in Brenchley, P., ed. Fossils and climate. Wiley, London.Google Scholar
Janis, C. M. 1988. An estimation of tooth volume and hypsodonty indices in ungulate mammals, and the correlation of these factors with dietary preferences. Pp. 367–387 in Russel, D. E., Santoro, J.-P., and Sigogneau-Russel, D., eds. Teeth revisited. Proceedings of the seventh international symposium on dental morphology, Paris.Google Scholar
Janis, C. M. 1990. The correlation between diet and dental wear in herbivorous mammals, and its relationship to the determination of diets of extinct species. Pp. 241–259 in Boucot, A. J., ed. Evolutionary paleobiology of behavior and coevolution. Elsevier, Amsterdam.Google Scholar
Janis, C. M. 1993. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics 24:467–500.Google Scholar
Janis, C. M. 1995. Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. Pp. 76–98 in Thomasson, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Janis, C. M. 1997/98. Ungulate teeth, diets, and climatic changes at the Eocene/Oligocene boundary. Zoology—Analysis of Complex Systems 100:203–220.Google Scholar
Janis, C. M., and Fortelius, M. 1988. On the means whereby mammals achieve increased functional durability of their dentitions with special reference to limiting factors. Biological Reviews of the Cambridge Philosophical Society 63:197–230.Google Scholar
Janis, C. M., Scott, K. M., and Jacobs, L. L. 1998. Evolution of Tertiary mammals in North America, Vol. 1. Terrestrial carnivores, ungulates, and ungulatelike mammals. Cambridge University Press, Cambridge.Google Scholar
Janis, C. M., Damuth, J., and Theodor, J. M. 2000. Miocene ungulates and terrestrial primary productivity: where have all the browsers gone? Proceedings of the National Academy of Sciences USA 97:237–261.Google Scholar
Janis, C. M., Damuth, J., and Theodor, J. M. 2002. The origins and evolution of the North American grassland biome: the story from the hoofed mammals. Palaeogeography, Palaeoclimatology, Palaeoecology 177:183–198.CrossRefGoogle Scholar
Janis, C. M., Damuth, J., and Theodor, J. M. 2004a. The species richness of Miocene browsers, and implications for habitat type and primary productivity in the North American grassland biome. Palaeogeography, Palaeoclimatology, Palaeoecology 207:371–398.Google Scholar
Janis, C. M., Errico, P., and Mendoza, M. 2004b. Morphological indicators of cursoriality in equids: legs fail to support the “arms race.” Journal of Vertebrate Paleontology 24:75A.Google Scholar
Jernvall, J., and Fortelius, M. 2002. Common mammals drive the evolutionary increase of hypsodonty in the Neogene. Nature 417:538–540.Google Scholar
Jernvall, J., Hunter, J. P., and Fortelius, M. 1996. Molar tooth diversity, disparity and ecology in Cenozoic ungulate radiations. Science 274:1489–1492.Google Scholar
Kay, R. F., and Covert, H. H. 1983. True grit: a microwear experiment. American Journal of Physical Anthropology 61:33–38.Google Scholar
Kellogg, E. A. 2001. Evolutionary history of the grasses. Plant Physiology 125:1198–1205.CrossRefGoogle ScholarPubMed
Kohlsdorf, T., Garland, T. J., and Navas, C. A. 2001. Limb and tail length in relation to substrate usage in Tropidurus lizards. Journal of Morphology 248:151–164.CrossRefGoogle ScholarPubMed
Kojola, I., Helle, T., Huhta, E., and Niva, A. 1998. Foraging conditions, tooth wear and herbivore body reserves: a study of female reindeer. Oecologia 117:26–30.Google Scholar
Kowalevsky, V. 1873. Sur L'Anchitherium aurelianense Cuv. et sur l'Histoire paleontologique des chevaux. Memoires de l'Académie Imperiale des Sciences de Saint-Petersbourg, VIIe series 20:1–73.Google Scholar
Kurtén, B. 1953. On the variation and population dymanics of fossil and recent mammal populations. Acta Zoologica Fennica 76:1–122.Google Scholar
Lander, B. 1998. Oreodontoidea. P. 691 in Janis, et al. 1998.Google Scholar
Lanyon, J. M., and Sanson, G. D. 1986. Koala (Phascolarctos cinereus) dentition and nutrition. II. Implications of tooth wear in nutrition. Journal of Zoology 209:169–181.Google Scholar
Lauder, G. V., Leroi, A. M., and Rose, M. R. 1993. Adaptations and history. Trends in Ecology and Evolution 8:294–297.Google Scholar
Leroi, A. M., Rose, M. R., and Lauder, G. V. 1994. What does the comparative method reveal about adaptation? American Naturalist 132:381–402.Google Scholar
Losos, J. B. 1999. Uncertainty in the reconstruction of ancestral character states and limitations on the use of phylogenetic comparative methods. Animal Behaviour 58:1319–1324.Google Scholar
Lucas, P. W., Turner, I. M., Dominy, N. J., and Yamashita, N. 2000. Mechanical defenses to herbivory. Annals of Botany 86:913–920.Google Scholar
MacFadden, B. J. 1977. Cladistic analysis of primitive equids, with notes on other perissodactyls. Systematic Zoology 25:1–14.Google Scholar
MacFadden, B. J. 1984. Systematics and phylogeny of Hipparion, Neohipparion, Nannippus, and Cormohipparion (Mammalia, Equidae) from the Miocene and Pliocene of the New World. Bulletin of the American Museum of Natural History 179:1–196.Google Scholar
MacFadden, B. J. 1985. Patterns of phylogeny and rates of evolution in fossil horses: hipparions from the Miocene and Pliocene of North America. Paleobiology 11:245–257.Google Scholar
MacFadden, B. J. 1988. Horses, the fossil record, and evolution: a current perspective. Pp. 131–158 in Hecht, M. K., Wallace, B., and Prance, G. T., eds. Evolutionary biology, Vol. 22. Plenum, New York.CrossRefGoogle Scholar
MacFadden, B. J. 1989. Dental character variation in paleopopulations and morphospecies of fossil horses and extant analogs. Pp. 128–141 in Prothero, and Schoch, 1989.Google Scholar
MacFadden, B. J. 1992. Fossil horses. Cambridge University Press, Cambridge.Google Scholar
MacFadden, B. J. 1997. Origin and evolution of the grazing guild in New World terrestrial mammals. Trends in Ecology and Evolution 12:182–187.Google Scholar
MacFadden, B. J. 1998. Equidae. Pp. 537–559 in Janis, et al. 1998.Google Scholar
MacFadden, B. J. 2000. Origin and evolution of the grazing guild in Cenozoic New World terrestrial mammals. Pp. 223–244 in Sues, H.-D., ed. Evolution of herbivory in terrestrial vertebrates: perspectives from the fossil record. Cambridge University Press, New York.Google Scholar
MacFadden, B. J. 2005. Fossil horses—evidence for evolution. Science 307:1728–1730.CrossRefGoogle ScholarPubMed
MacFadden, B. J., and Cerling, T. E. 1994. Fossil horses, carbon isotopes and global change. Trends in Ecology and Evolution 9:481–486.Google Scholar
MacFadden, B. J., and Hunt, R. M. Jr. 1998. Magnetic polarity stratigraphy and correlation of the Arikaree Group, Arikareean (late Oligocene-early Miocene) of northwestern Nebraska. In Terry, D. O., LaGarry, H. E., and Hunt, R. M. Jr., eds. Depositional environments, lithostratigraphy, and biostratigraphy of the White River Group and Arikaree Groups (Late Eocene to Early Miocene, North America). Geological Society of America Special Paper 325:143–165.Google Scholar
MacFadden, B. J., Bryant, J. D., and Mueller, P. A. 1991. Sr-iso-topic, paleomagnetic, and biostratigraphic calibration of horse evolution: evidence from the Miocene of Florida. Geology 19:242–245.Google Scholar
MacFadden, B. J., Solounias, N., and Cerling, T. E. 1999. Ancient diets, ecology, and extinction of 5-million-year-old horses from Florida. Science 283:824–827.Google Scholar
Martins, E. P. 2000. Adaptation and the comparative method. Trends in Ecology and Evolution 15:296–299.Google Scholar
Martins, E. P., and Hansen, T. F. 1996. The statistical analysis of interspecific data: a review and evaluation of phylogenetic comparative methods. Pp. 22–75 in Martins, E. P., ed. Phylogenies and the comparative method in animal behavior. Oxford University Press, New York.CrossRefGoogle Scholar
Matthew, W. D. 1926. The evolution of the horse: a record and its interpretation. Quarterly Review of Biology 1:139–185.Google Scholar
Mayr, E. 1963. Animal species and evolution. Harvard University Press, Cambridge.Google Scholar
McNaughton, S. J., and Tarrants, J. L. 1983. Grass leaf silicification: natural selection for an inducible defense against herbivores. Proceedings of the National Academy of Sciences USA 80:790–791.Google Scholar
McNaughton, S. J., Tarrants, J. L., McNaughton, M., and Davis, R. H. 1985. Silica as a defense against herbivory and a growth promotor in African grasses. Ecology 66:528–535.Google Scholar
Mess, A., Mohr, B., and Martin, T. 2001. Evolutionary transformations of hystricognath Rodentia and the climatic change in the Eocene to Late Oligocene time interval. Mitteilungen aus dem Museum für Naturkunde zu Berlin, Zoologische Reihe 77:193–206.Google Scholar
Mishler, B. D. 1988. Reproductive ecology of bryophytes. Pp. 285–306 in Doust, J. L. and Doust, L. L., eds. Plant reproductive ecology: patterns and strategies. Oxford University Press, Oxford.Google Scholar
Nichols, R., Tabrum, A. R., Barnosky, A. D., and Hill, C. L. 2001. Cenozoic vertebrate paleontology and geology of southwestern Montana and adjacent areas. Pp. 77–144 in Hill, C. L., ed. Mesozoic and Cenozoic paleontology in the Western Plains and Rocky Mountains. Guidebook for the field trips. Society of Vertebrate Paleontology 61st annual meeting. Museum of the Rockies, Bozeman, Mont. Google Scholar
Osborn, H. F. 1910. The age of mammals in Europe, Asia and North America. Macmillan, New York.Google Scholar
Padian, K. 1987. A comparative phylogenetic and functional approach to the origin of vertebrate flight. Pp. 3–22 in Fenton, M. B., Racey, P., and Rayner, J. M. V., eds. Recent advances in the study of bats. Cambridge University Press, Cambridge.Google Scholar
Pérez-Barbería, F. J., and Gordon, I. J. 1998a. Factors affecting food comminution during mastication in herbivorous mammals: a review. Biological Journal of the Linnean Society 63:233–256.Google Scholar
Pérez-Barbería, F. J., and Gordon, I. J. 1998b. The influence of molar occlusal surface area on the voluntary intake, digestion, chewing behaviour and diet selection of red deer (Cervus elaphus). Journal of Zoology 245:307–316.Google Scholar
Peyer, B. 1968. Comparative odontology. University of Chicago Press, Chicago.Google Scholar
Pfister, C. A. 1998. Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. Proceedings of the National Academy of Sciences USA 95:213–218.Google Scholar
Pfretzschner, H. U. 1992. Enamel microstructure and hypsodonty in large mammals. Pp. 147–162 in Smith, P. and Tchernov, E., eds. Structure, function and evolution of teeth. Freund Publishing House, Tel Aviv.Google Scholar
Pfretzschner, H. U. 1993. Enamel microstructure in the phylogeny of the Equidae. Journal of Vertebrate Paleontology 13:342–349.Google Scholar
Piperno, D. R., and Pearsall, D. M. 1998. The silica bodies of tropical American grasses: morphology, taxonomy, and implications for grass systematics and fossil phytolith identification. Smithsonian Contributions to Botany 85:1–40.Google Scholar
Potts, R., and Behrensmeyer, A. K. 1992. Late Cenozoic terrestrial ecosystems. Pp. 419–541 in Behrensmeyer, A. K., Damuth, J. D., DiMichele, W. A., Potts, R., Sues, H.-D., and Wing, S. L., eds. Terrestrial ecosystems through time: evolutionary paleoecology of terrestrial plants and animals. University of Chicago Press, Chicago.Google Scholar
Prothero, D. R. 1998a. Hyracodontidae. Pp. 589–594 in Janis, et al. 1998.Google Scholar
Prothero, D. R. 1998b. Rhinocerotidae. Pp. 595–605 in Janis, et al. 1998.Google Scholar
Prothero, D. R. 1998c. The chronological, climatic, and paleogeographic background to North American mammalian evolution. Pp. 9–36 in Janis, et al. 1998.Google Scholar
Prothero, D. R., and Schoch, R. M., eds. 1989. The evolution of perissodactyls. Oxford University Press, New York.Google Scholar
Prothero, D. R., and Shubin, N. 1989. The evolution of Oligocene horses. Pp. 142–175 in Prothero, and Schoch, 1989.Google Scholar
Prothero, D. R., and Whittlesey, K. E. 1998. Magnetic stratigraphy and biostratigraphy of the Orellan and Whitneyan land-mammal “ages” in the White River Group. In Terry, D. O., LaGarry, H. E., and Hunt, R. M. Jr., eds. Depositional environments, lithostratigraphy, and biostratigraphy of the White River Group and Arikaree Groups (Late Eocene to Early Miocene, North America). Geological Society of America Special Paper 325:39–61.Google Scholar
Prothero, D. R., Manning, E., and Hanson, C. B. 1986. The phylogeny of the Rhinocerotoidea (Mammalia, Perissodactyla). Zoological Journal of the Linnean Society 87:341–366.Google Scholar
Prothero, D. R., Guérin, C., and Manning, E. 1989. The history of the Rhinocerotoidea. Pp. 321–340 in Prothero, and Schoch, 1989.Google Scholar
Radinsky, L. 1983. Allometry and reorganization in horse skull proportions. Science 221:1189–1191.Google Scholar
Radinsky, L. 1984. Ontogeny and phylogeny in horse skull evolution. Evolution 38:1–15.Google Scholar
Rensberger, J. M. 1973. An occlusion model for mastication and dental wear in herbivorous mammals. Journal of Paleontology 47:515–528.Google Scholar
Rensberger, J. M., Forstén, A.-M., and Fortelius, M. 1984. Functional evolution of the cheek tooth pattern and chewing direction in Tertiary horses. Paleobiology 10:439–452.Google Scholar
Retallack, G. J. 2001. Cenozoic expansion of grasslands and climatic cooling. Journal of Geology 109:407–426.Google Scholar
Schluter, D., Price, T., Mooers, A. Ø., and Ludwig, D. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711.Google Scholar
Scott, W. B. 1937. A history of land mammals in the western hemisphere. Macmillan, New York.Google Scholar
Simpson, G. G. 1944. Tempo and mode in evolution. Columbia University Press, New York.Google Scholar
Simpson, G. G. 1951. Horses: The story of the horse family in the modern world and through sixty million years of history. Oxford University Press, Oxford.Google Scholar
Skogland, T. 1988. Tooth wear by food limitation and its life-history consequences in wild reindeer. Oikos 51:238–242.Google Scholar
Solounias, N., and Moellecken, S. M. C. 1993. Dietary adaptation of some extinct ruminants determined by premaxillary shape. Journal of Mammalogy 74:1059–1071.Google Scholar
Solounias, N., and Semprebon, G. M. 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. American Museum Novitates:1–49.Google Scholar
Solounias, N., Fortelius, M., and Freeman, P. 1994. Molar wear rates in ruminants: a new approach. Annales Zoologici Fennici 31:219–227.Google Scholar
Solounias, N., Moellecken, S. M. C., and Plavcan, J. M. 1995. Predicting the diet of extinct bovids using masseteric morphology. Journal of Vertebrate Paleontology 15:795–805.Google Scholar
Stebbins, G. L. 1981. Coevolution of grasses and herbivores. Annals of the Missouri Botanical Garden 68:75–86.Google Scholar
Stirton, R. A. 1947. Observations on evolutionary rates in hypsodonty. Evolution 1:34–41.CrossRefGoogle Scholar
Strömberg, C. A. E. 2002. The origin and spread of grass-dominated ecosystems in the Late Tertiary of North America: preliminary results concerning the evolution of hypsodonty. Palaeogeography Palaeoclimatology Palaeoecology 177:59–75.Google Scholar
Strömberg, C. A. E. 2004. Using phytolith assemblages to reconstruct the origin and spread of grass-dominated habitats in the Great Plains during the late Eocene to early Miocene. Palaeogeography, Palaeoclimatology, Palaeoecology 207:239–275.Google Scholar
Strömberg, C. A. E. 2005. Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Sciences USA 102:11980–11984.Google Scholar
Swinehart, J. B., Souders, V. L., DeGraw, H. M., and Diffendal, R. F. J. 1985. Cenozoic paleogeography of Western Nebraska. Pp. 209–229 in Flores, R. M. and Kaplan, S. S., eds. Cenozoic paleogeography of West-Central United States. Rocky Mountain Paleogeography Symposium no. 3. Rocky Mountain Section. Society of Economic Paleontologists and Mineralogists, Tulsa, Okla. Google Scholar
Teaford, M. F. 1988. A review of dental microwear and diet in modern mammals. Scanning Microscopy 2:1149–1166.Google Scholar
Van Valen, L. 1960. A functional index of hypsodonty. Evolution 14:531–532.Google Scholar
Van Valen, L. 1963. Selection in natural populations: Merychippus primus, a fossil horse. Nature 4873:1181–1183.Google Scholar
Van Valen, L. 1964. Age in two fossil horse populations. Acta Zoologica 45:93–106.Google Scholar
Van Valen, L. 1965. Selection in natural populations. III. Measurement and estimation. Evolution 19:514–528.Google Scholar
Vicari, M., and Bazely, D. R. 1993. Do grasses fight back? The case for antiherbivore defenses. Trends in Ecology and Evolution 8:137–141.Google Scholar
Wake, D. B., Roth, G., and Wake, M. H. 1983. On the problem of stasis in organismal evolution. Journal of Theoretical Biology 101:211–224.Google Scholar
Walker, A., Hoecke, H. N., and Perez, L. 1978. Microwear of mammalian teeth as an indicator of diet. Science 201:908–910.Google Scholar
Wang, Y., Cerling, T. E., MacFadden, B. J., and Bryant, J. D. 1994. Fossil horses and carbon isotopes: new evidence for Cenozoic dietary, habitat, and ecosystem changes in North America. Palaeogeography, Palaeoclimatology, Palaeoecology 107:269–280.Google Scholar
Webb, S. D. 1977. A history of savanna vertebrates in the New World. Annual Review of Ecology and Systematics 8:355–380.Google Scholar
Webb, S. D. 1983. The rise and fall of the late Miocene ungulate fauna in North America. Pp. 267–306 in Nitecki, M. H., ed. Coevolution. University of Chicago Press, Chicago.Google Scholar
Webb, S. D., and Opdyke, N. D. 1995. Global climatic influence on Cenozoic land mammal faunas. Pp. 184–208 in Kennett, J. and Stanley, S., eds. Effects of past global change on life. National Academy Press, Washington, D.C. Google Scholar
Williams, G. C. 1966. Adaptation and natural selection. Princeton University Press, Princeton, N.J. Google Scholar
Williams, S. H., and Kay, R. F. 2001. A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution 8:207–229.Google Scholar
Wilson, E. O. 1975. Sociobiology: the new synthesis. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Wilson, J. R., and Hacker, J. B. 1987. Comparative digestibility and anatomy of some sympatric C3 and C4 arid zone grasses. Australian Journal of Agricultural Research 38:287–295.Google Scholar
Wilson, J. R., and Kennedy, P. M. 1996. Plant and animal constraints to voluntary feed-intake associated with fiber characteristics and particle breakdown and passage in ruminants. Australian Journal of Agricultural Research 47:199–225.Google Scholar
Wilson, J. R., Deinum, B., and Engels, F. M. 1991. Temperature effects on anatomy and digestibility of leaf and stem of tropical and temperate forage species. Netherlands Journal of Agricultural Science 39:31–48.Google Scholar
Wing, S. L. 1998. Tertiary vegetation of North America as a context for mammalian evolution. Pp. 37–65 in Janis, et al. 1998.Google Scholar
Woodburne, M. O. 1987. Cenozoic mammals of North America. University of California Press, Berkeley.Google Scholar
Woodburne, M. O., ed. 2004. Late Cretaceous and Cenozoic mammals of North America: biostratigraphy and geochronology. Columbia University Press, New York.Google Scholar