Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2025-01-03T23:39:06.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Do convergent ecomorphs evolve through convergent morphological pathways? Cranial shape evolution in fossil hyaenids and borophagine canids (Carnivora, Mammalia)

Published online by Cambridge University Press:  08 April 2016

Zhijie Jack Tseng  and
Xiaoming Wang
Zhijie Jack Tseng
Affiliation:
Integrative and Evolutionary Biology Program, Department of Biological Sciences, 3616 Trousdale Parkway, University of Southern California, Los Angeles, California 90089 Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007. E-mail: jtseng@nhm.org
Xiaoming Wang
Affiliation:
Department of Vertebrate Paleontology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007
Get access Rights & Permissions [Opens in a new window]

Abstract

Cases of convergent evolution, particularly within ecomorphological contexts, are instructive in identifying universally adaptive morphological features across clades. Tracing of evolutionary pathways by which ecomorphological convergence takes place can further reveal mechanisms of adaptation, which may be strongly influenced by phylogeny. Ecomorphologies of carnivorous mammals represent some of the most outstanding cases of convergent evolution in the Cenozoic radiation of mammals. This study examined patterns of cranial shape change in the dog (Canidae) and hyena (Hyaenidae) families, in order to compare the evolutionary pathways that led to the independent specialization of bone-cracking hypercarnivores within each clade. Geometric morphometrics analyses of cranial shape in fossil hyaenids and borophagine canids provided evidence for deep-time convergence in morphological pathways toward the independent evolution of derived bone-crackers. Both clades contained stem members with plesiomorphic generalist/omnivore cranial shapes, which evolved into doglike species along parallel pathways of shape change. The evolution of specialized bone-crackers from these doglike forms, however, continued under the constraint of a full cheek dentition and restriction on rostrum length reduction in canids, but not hyaenids. Functionally, phylogenetic constraint may have limited borophagine canids to crack bones principally with their carnassial instead of the third premolar as in hyaenids, but other cranial shape changes associated with durophagy nevertheless evolved in parallel in the two lineages. Size allometry was not a major factor in cranial shape evolution in either lineage, supporting the interpretation of functional demands as drivers for the observed convergence. The comparison between borophagines and hyaenids showed that differential effects of alternative functional “solutions” that arise during morphological evolution may be multiplied with processes of the “macroevolutionary ratchet” already in place to further limit the evolutionary pathways available to specialized lineages.

Type
Articles
Information
Paleobiology , Volume 37 , Issue 3 , Summer 2011 , pp. 470 - 489
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

Adams, D. C., Rohlf, F. J., and Slice, D. E. 2004. Geometric morphometrics: ten years of progress following the ‘Revolution.’ Italian Journal of Zoology 71:5–16.CrossRefGoogle Scholar
Andersson, K. 2005. Were there pack-hunting canids in the Tertiary, and how can we know? Paleobiology 31:56–72.2.0.CO;2>CrossRefGoogle Scholar
Berta, A. 1981. The Plio-Pleistocene hyaena Chasmaporthetes ossifragus from Florida. Journal of Vertebrate Paleontology 1:341–356.CrossRefGoogle Scholar
Binder, W. J., and Van Valkenburgh, B. 2000. Development of bite strength and feeding behavior in juvenile spotted hyenas (Crocuta crocuta). Journal of the Zoological Society of London 252:273–283.CrossRefGoogle Scholar
Bookstein, F. L. 1991. Morphometric tools for landmarks data. Cambridge University Press, London.Google Scholar
Carbone, C., Mace, G. M., Roberts, S. C., and Macdonald, D. W. 1999. Energetic constraints on the diet of terrestrial carnivores. Nature 402:286–288.CrossRefGoogle ScholarPubMed
Christiansen, P. 2008. Evolution of skull and mandible shape in cats (Carnivora: Felidae). PLoS ONE 3(7):e2807.CrossRefGoogle ScholarPubMed
Crusafont-Pairó, M. 1950. El primer representante del género Canis en el Pontiense eurasiatico (Canis cipio nova sp.). Boletín de la Real Sociedad Española de Historia Natural (Geologia) 48:43–51.Google Scholar
Crusafont-Pairó, M., and Truyols-Santonja, J. 1956. A biometric study of the evolution of fissiped carnivores. Evolution 10:314–332.CrossRefGoogle Scholar
de Bonis, L., Peigne, S., Likius, A., Mackaye, H. T., Vignaud, P., and Brunet, M. 2007. The oldest African fox (Vulpes riffautae n. sp., Canidae, Carnivora) recovered in late Miocene deposits of the Djurab desert, Chad. Naturwissenschaften 94:575–580.CrossRefGoogle Scholar
Ellis, J. L., Thomason, J. J., Kebreab, E., Zubair, K., and France, J. 2009. Cranial dimensions and forces of biting in the domestic dog. Journal of Anatomy 214:362–373.CrossRefGoogle ScholarPubMed
Ewer, R. F. 1973. The carnivores. Cornell University Press, Ithaca, N.Y.Google Scholar
Ferretti, M. P. 1999. Tooth enamel structure in the hyaenid Chasmaporthetes lunensis lunensis from the late Pliocene of Italy, with implications for feeding behavior. Journal of Vertebrate Paleontology 19:767–770.CrossRefGoogle Scholar
Ferretti, M. P. 2007. Evolution of bone-cracking adaptations in hyaenids (Mammalia, Carnivora). Swiss Journal of Geoscience 100:41–52.CrossRefGoogle Scholar
Figueirido, B., Palmqvist, P., and Perez-Claros, J. A. 2009. Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics. Journal of Zoology 277:70–80.CrossRefGoogle Scholar
Gould, S. J. 1966. Allometry and size in ontogeny and phylogeny. Biology Review 41:587–640.CrossRefGoogle ScholarPubMed
Greaves, W. S. 1983. A functional analysis of carnassial biting. Biological Journal of the Linnean Society 20:353–364.CrossRefGoogle Scholar
Greaves, W. S. 1985. The generalized carnivore jaw. Zoological Journal of the Linnean Society 85:267–274.CrossRefGoogle Scholar
Greaves, W. S. 2000. Location of the vector of jaw muscle force in mammals. Journal of Morphology 243:293–299.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Hay, O. P. 1921. Descriptions of species of Pleistocene Vertebrata, types or specimens most of which are preserved in the United States National Museum. Proceedings of the United States National Museum 59:599–642.CrossRefGoogle Scholar
Holliday, J. A., and Steppan, S. J. 2004. Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity. Paleobiology 30:108–128.2.0.CO;2>CrossRefGoogle Scholar
Jenks, S. M., and Werdelin, L. 1998. Taxonomy and systematics of living hyaenas (Family Hyaenidae). IUCN/SSC Hyaena Specialist Group, Gland, Switzerland.Google Scholar
Koepfli, K.-P., Jenks, S. M., Eizirik, E., Zahirpour, T., Van Valkenburgh, B., and Wayne, R. K. 2006. Molecular systematics of the Hyaenidae: relationships of a relictual lineage resolved by a molecular supermatrix. Molecular Phylogenetics and Evolution 38:603–620.CrossRefGoogle ScholarPubMed
Kruuk, H. 1972. The spotted hyena: a study of predation and social behavior. University of Chicago Press, Chicago.Google Scholar
Kurtén, B. 1968. Pleistocene Mammals of Europe. Weindenfeld and Nicholson, London.Google Scholar
Kurtén, B., and Werdelin, L. 1988. A review of the genus Chasmaporthetes Hay, 1921 (Carnivora, Hyaenidae). Journal of Vertebrate Paleontology 8:46–66.CrossRefGoogle Scholar
Lauder, G. V. 1995. On the inference of function from structure. Pp. 9–18 in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Lauder, G. V. 1996. The argument from design. Pp. 55–91 in Rose, M. R. and Lauder, G. V., eds. Adaptation. Academic Press, San Diego.Google Scholar
Maddison, W. P., and Maddison, D. R. 2009. Mesquite: a modular system for evolutionary analysis, Version 2.72. http://mesquiteproject.org Google Scholar
Martin, L. D. 1989. Chapter 19. Fossil history of the terrestrial Carnivora. Pp. 536–568 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, New York.CrossRefGoogle Scholar
McHenry, C., Wroe, S., Clausen, P. D., Moreno, K., and Cunningham, E. 2007. Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation. Proceedings of the National Academy of Sciences USA 104:16010–16015.CrossRefGoogle ScholarPubMed
Meloro, C., Raia, P., Piras, P., Barbera, C., and O'Higgins, P. 2008. The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zoological Journal of Linnean Society 154:832–845.CrossRefGoogle Scholar
Midford, P. E., Garland, T. Jr., and Maddison, W. P. 2008. PDAP package of Mesquite, Version 1.14. http://mesquiteproject.org/pdap_mesquite/ Google Scholar
Mills, M. G. L. 1990. Kalahari hyenas: comparative behavioral ecology of two species. Blackburn Press, Caldwell, N.J.CrossRefGoogle Scholar
Mills, M. G. L., and Mills, M. E. J. 1978. The diet of the brown hyaena Hyaena brunnea in the southern Kalahari. Koedoe 21:125–149.CrossRefGoogle Scholar
Munthe, K. 1989. The skeleton of the Borophaginae (Carnivora, Canidae), morphology and function. University of California Publications Bulletin of the Department of Geological Sciences 133:1–115.Google Scholar
Qiu, Z.-X., ed. 2003. Dispersals of Neogene carnivorans between Asia and North America. American Museum of Natural History, New York.Google Scholar
Raia, P. 2004. Morphological correlates of tough food consumption in large land carnivores. Italian Journal of Zoology 71:45–50.CrossRefGoogle Scholar
Rohlf, F. J. 2005. tpsRegr, Version 1.31. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Rohlf, F. J. 2006a. tpsDig, digitize landmarks and outlines, Version 2.05. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Rohlf, F. J. 2006b. tpsRelw, Version 1.44. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Sheets, H. D. 2004. Integrated morphometrics package. Department of Physics, Canisius College, Buffalo, N.Y. Google Scholar
Slater, G. J., and Van Valkenburgh, B. 2008. Long in the tooth: evolution of sabertooth at cranial shape. Paleobiology 34:403–419.CrossRefGoogle Scholar
Stayton, C. T. 2006. Testing hypotheses of convergence with multivariate data: morphological and functional convergence among herbivorous lizards. Evolution 60:824–841.Google ScholarPubMed
Stefen, C. 1999. Enamel microstructure of recent and fossil Canidae (Carnivora: Mammalia). Journal of Vertebrate Paleontology 19:576–587.CrossRefGoogle Scholar
Stefen, C., and Rensberger, J. M. 2002. The specialized enamel structure of hyaenids (Mammalia, Hyaenidae): description and development within the lineage—including percrocutids. Zoologische Abhandlungen 52:127–147.Google Scholar
Tanner, J. B., Dumont, E. R., Sakai, S. T., Lundrigan, B. L., and Holekamp, K. E. 2008. Of arcs and vaults: the biomechanics of bone-cracking in spotted hyenas (Crocuta crocuta). Biological Journal of the Linnean Society 95:246–255.CrossRefGoogle Scholar
Tanner, J. B., Zelditch, M., Lundrigran, B. L., and Holekamp, K. E. 2010. Ontogenetic change in skull morphology and mechanical advantage in the spotted hyena (Crocuta crocuta). Journal of Morphology 271:353–365.CrossRefGoogle ScholarPubMed
Tedford, R. H., Wang, X., and Taylor, B. E. 2009. Phylogenetic systematics of the North American fossil Caninae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 325:1–218.CrossRefGoogle Scholar
Tseng, Z. J. 2009. Cranial function in a late Miocene Dinocrocuta gigantea (Mammalia: Carnivora) revealed by comparative finite element analysis. Biological Journal of the Linnean Society 96:51–67.CrossRefGoogle Scholar
Tseng, Z. J., and Wang, X. 2010. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). Journal of Morphology 271:1386–1398.CrossRefGoogle ScholarPubMed
Turner, A., and Anton, M. 1996. The giant hyaena, Pachycrocuta brevirostris (Mammalia, Carnivora, Hyaenidae). Geobios 29:455–468.CrossRefGoogle Scholar
Turner, A., Anton, M., and Werdelin, L. 2008. Taxonomy and evolutionary patterns in the fossil Hyaenidae of Europe. Geobios 41:677–687.CrossRefGoogle Scholar
Van Valkenburgh, B. 1985. Locomotor diversity within past and present guilds of large predatory mammals. Paleobiology 11:406–428.CrossRefGoogle Scholar
Van Valkenburgh, B. 1988. Trophic diversity in past and present guilds of large predatory mammals. Paleobiology 14:155–173.CrossRefGoogle Scholar
Van Valkenburgh, B. 1989. Carnivore dental adaptations and diet: a study of trophic diversity within guilds. Pp. 410–436 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, New York.CrossRefGoogle Scholar
Van Valkenburgh, B. 1991. Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): evolutionary interactions among sympatic predators. Paleobiology 17:340–362.CrossRefGoogle Scholar
Van Valkenburgh, B. 1995. Tracking ecology over geological time: evolution within guilds of vertebrates. Trends in Ecology and Evolution 10:71–76.CrossRefGoogle Scholar
Van Valkenburgh, B. 1999. Major patterns in the history of carnivorous mammals. Annual Review of Earth and Planetary Science 27:463–493.CrossRefGoogle Scholar
Van Valkenburgh, B. 2001. Chapter 5. The dog-eat-dog world of carnivores: a review of past and present carnivore community dynamics. Pp. 101–121 in Stanford, C. B. and Bunn, H. T., eds. Meat eating and hominid evolution. Oxford University Press, New York.CrossRefGoogle Scholar
Van Valkenburgh, B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47:147–163.CrossRefGoogle ScholarPubMed
Van Valkenburgh, B., and Koepfli, K.-P. 1993. Cranial and dental adaptations to predation in canids. Symposium of the Zoological Society of London 65:15–37.Google Scholar
Van Valkenburgh, B., and Molnar, R. E. 2002. Dinosaurian and mammalian predators compared. Paleobiology 28:527–543.2.0.CO;2>CrossRefGoogle Scholar
Van Valkenburgh, B., Wang, X., and Damuth, J. 2004. Cope's Rule, hypercarnivory, and extinction in North American canids. Science 306(5693):101–104.CrossRefGoogle ScholarPubMed
Wang, X. 1994. Phylogenetic systematics of the Hesperocyoninae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 221:1–207.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 243:1–391.Google Scholar
Wang, X., Tedford, R. H., and Anton, M. 2008. The dog family, Canidae, and their evolutionary history. Columbia University Press, New York.Google Scholar
Werdelin, L. 1989. Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology 15:387–401.CrossRefGoogle Scholar
Werdelin, L. 1996. Chapter 17. Carnivoran ecomorphology: a phylogenetic perspective. Pp. 582–624 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, New York.Google Scholar
Werdelin, L., and Solounias, N. 1991. The Hyaenidae: taxonomy, systematics and evolution. Fossils and Strata 30:1–104.CrossRefGoogle Scholar
Werdelin, L., and Solounias, N. 1996. The evolutionary history of hyenas in Europe and western Asia during the Miocene. Pp. 290–306 in Bernor, R. L., Fahlbusch, V., and Rietschel, S., eds. Later Neogene European biotic evolution and stratigraphic correlation. Columbia University Press, New York.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 Carnivora. Journal of Systematic Paleontology 3:1–28.CrossRefGoogle Scholar
Zanno, L. E., Gillete, D. D., Albright, L. B. III, and Titus, A. L. 2009. A new North American therizinosaurid and the role of herbivory in ‘predatory’ dinosaur evolution. Proceedings of the Royal Society of London B 276:3503–3511.Google ScholarPubMed
Zelditch, M., Swiderski, D., Sheets, D., and Fink, W. 2004. Geometric morphometrics for biologists. Elsevier, New York.Google Scholar