Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-18T11:13:11.978Z Has data issue: false hasContentIssue false
  • English
  • Français

The time of origin of whales and the role of behavioral changes in the terrestrial-aquatic transition

Published online by Cambridge University Press:  08 February 2016

Maureen A. O'Leary  and
Mark D. Uhen
Maureen A. O'Leary
Affiliation:
Department of Anatomical Sciences, Health Sciences Center, Tower 8 (040), State University of New York at Stony Brook, Stony Brook, New York 11794-8081. E-mail: moleary@mail.som.sunysb.edu
Mark D. Uhen
Affiliation:
Cranbrook Institute of Science, Bloomfield Hills, Michigan 48303-0801. E-mail: muhen@pop.cranbrook.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Addition of the recently discovered fossil Nalacetus to a phylogenetic analysis of basicranial, cranial, dental, postcranial, and soft morphological characters reveals that it is the most basal cetacean, and that mesonychians form the monophyletic sister group to Cetacea. The molars of Nalacetus elucidate transformations in dental morphology that occurred early in the cetacean radiation and clarify certain derived differences in molar cusp position between cetaceans and the extinct clade, Mesonychia, hypothesized to be their sister taxon. Nalacetus and other archaic cetaceans share derived vertically elongate shearing facets on the lower molars. Applying the Extant Phylogenetic Bracket, we advance the hypothesis that these facets are an osteological correlate of aquatic predation. Our functional interpretation of this character and its distribution within Cetacea indicates that a behavioral change in tooth use characterized the origin of the clade. Comparison of the transformation of this dental character with that of the cetacean pelvis indicates that a change in tooth use (feeding behavior) occurred before loss of the ability to engage in terrestrial locomotion.

The most parsimonious phylogenetic hypothesis presented here has a significant fit with the stratigraphic record as determined by the Manhattan Stratigraphic Measure, which is corroborated by retention indices of stratigraphic data. Ghost lineages necessitated by the phylogenetic hypothesis extend the stratigraphic range of Cetacea into the middle Paleocene (Torrejonian), ten million years earlier than the oldest cetacean fossil currently known. Primitive features of Nalacetus, the large number of synapomorphies diagnosing Cetacea, and the implied ghost lineage suggest that the early cetacean radiation was much more extensive than has been previously recognized.

Type
Articles
Information
Paleobiology , Volume 25 , Issue 4 , Fall 1999 , pp. 534 - 556
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

Bajpai, S., and Gingerich, P. D. 1998. A new Eocene archaeocete (Mammalia, Cetacea) from India and the time of origin of whales. Proceedings of the National Academy of Sciences USA 95:15464–15468.CrossRefGoogle ScholarPubMed
Barnes, L. G. 1984. Whales, dolphins and porpoises: origin and evolution of the Cetacea. In Gingerich, P. D. and Badgely, C. E., eds. Mammals: notes for a short course. Studies in Geology 8(1–4):139–154. Department of Geological Sciences, University of Tennessee, Knoxville.Google Scholar
Benton, M. J., and Hitchin, R. 1996. Testing the quality of the fossil record by groups and by major habitats. Historical Biology 12:111–157.CrossRefGoogle Scholar
Berta, A. 1994. What is a whale? Science 263:180–181.CrossRefGoogle ScholarPubMed
Carroll, R. L. 1997. Patterns and processes of vertebrate evolution. Cambridge University Press, Cambridge.Google Scholar
Cifelli, R. L. 1982. The petrosal structure of Hyopsodus with respect to that of some other ungulates, and its phylogenetic implications. Journal of Paleontology 56:795–805.Google Scholar
Clyde, W. C., and Fisher, D. C. 1997. Comparing the fit of stratigraphic and morphologic data in phylogenetic analysis. Paleobiology 23:1–19.CrossRefGoogle Scholar
DeBraga, M., and Carroll, R. L. 1993. The origin of mosasaurs as a model of macroevolutionary patterns and processes. Evolutionary Biology 27:245–322.Google Scholar
Fisher, D. C. 1992. Stratigraphic parsimony. Pp. 124–129in Maddison, W. P. and Maddison, D. R.MacClade: analysis of phylogeny and character evolution, Version 3. Sinauer, Sunderland, Mass.Google Scholar
Foote, M., Hunter, J. P., Janis, C. M., and Sepkoski, J. J. Jr. 1999. Evolutionary and preservation constraints on origins of biologic groups: divergence times of eutherian mammals. Science 283:1310–1314.CrossRefGoogle ScholarPubMed
Gatesy, J. 1997. More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene γ-fibrinogen. Molecular Biology and Evolution 14:537–543.CrossRefGoogle ScholarPubMed
Gatesy, J. 1998. Molecular evidence for the phylogenetic affinities of Cetacea. Pp. 63–111in Thewissen, 1998.Google Scholar
Gatesy, J., Hayashi, C., Cronin, M. A., and Arctander, P. 1996. Evidence from milk casein genes that cetaceans are close relatives of hippopotamid artiodactyls. Molecular Biology and Evolution 13:954–963.CrossRefGoogle ScholarPubMed
Gauthier, J., Kluge, A. G., and Rowe, T. 1988. Amniote phylogeny and the importance of fossils. Cladistics 4:105–209.CrossRefGoogle ScholarPubMed
Geisler, J. H., and Luo, Z. 1996. The petrosal and inner ear of Herpetocetus sp. (Mammalia, Cetacea) and their implications for the phylogeny and hearing of archaic mysticetes. Journal of Paleontology 70:1045–1066.CrossRefGoogle Scholar
Geisler, J. H., and Luo, Z. 1998. Relationships of Cetacea to terrestrial ungulates and the evolution of cranial vasculature in Cete. Pp. 163–212in Thewissen, 1998.Google Scholar
Gentry, A. W., and Hooker, J. J. 1988. The phylogeny of the Artiodactyla. In Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 2. Mammals. Systematics Association Special Volume 35B:235–272. Clarendon, Oxford.Google Scholar
Gingerich, P. D., and Uhen, M. D. 1998. Likelihood estimation of the time of origin of Cetacea and the time of divergence of Cetacea and Artiodactyla. Palaeontologia Electronica 1:1–28 [http://www-odp.tamu.edu/paleo/1998_2/ging_uhen/issue2.htm].Google Scholar
Gingerich, P. D., Smith, B. H., and Simons, E. L. 1990. Hind limbs of Eocene Basilosaurus: evidence of feet in whales. Science 249:154–157.CrossRefGoogle ScholarPubMed
Gingerich, P. D., Arif, M., and Clyde, W. C. 1995. New archaeocetes (Mammalia, Cetacea) from the middle Eocene Domanda Formation of the Sulaiman Range; Punjab (Pakistan). Contributions from the Museum of Paleontology, University of Michigan 29: 291–230.Google Scholar
Hitchin, R., and Benton, M. J. 1997a. Congruence between parsimony and stratigraphy: comparisons of three indices. Paleobiology 23:20–32.CrossRefGoogle Scholar
Hitchin, R., and Benton, M. J. 1997b. Stratigraphic indices and tree balance. Systematic Biology 46:563–569.CrossRefGoogle Scholar
Huelsenbeck, J. P. 1994. Comparing the stratigraphic record to estimates of phylogeny. Paleobiology 20:470–483.CrossRefGoogle Scholar
Kumar, S., and Hedges, B. 1998. A molecular timescale for vertebrate evolution. Nature 392:917–920.CrossRefGoogle ScholarPubMed
Langer, P. 1988. The mammalian herbivore stomach: comparative anatomy, function and evolution. Fischer, Stuttgart.Google Scholar
Losos, J. B. 1996. Phylogenies and comparative biology, stage II: testing causal hypotheses derived from phylogenies with data from extant taxa. Systematic Biology 45:259–260.CrossRefGoogle Scholar
Luckett, W. P., and Hong, N. 1998. Phylogenetic relationships between the orders Artiodactyla and Cetacea: a combined assessment of morphological and molecular evidence. Journal of Mammalian Evolution 5:127–182.CrossRefGoogle Scholar
Luo, Z. 1998. Homology and transformation of cetacean ectotympanic structures. Pp. 269–301in Thewissen, 1998.Google Scholar
Luo, Z., and Marsh, K. 1996. Petrosal (periotic) and inner ear of a Pliocene kogiine whale (Kogiinae, Odontoceti): implications on relationships and hearing evolution of toothed whales. Journal of Vertebrate Paleontology 16:328–348.CrossRefGoogle Scholar
MacLeod, N., and Rose, K. D. 1993. Inferring locomotor behavior in Paleogene mammals via eigenshape analysis. American Journal of Science 293-A:300–355.CrossRefGoogle Scholar
MacPhee, R. D. E. 1981. Auditory regions of primates and eutherian insectivores: morphology, ontogeny, and character analysis. Contributions to Primatology 18:1–282.Google Scholar
MacPhee, R. D. E. 1994. Morphology, adaptations, and relationships of Plesiorycteropus, and a diagnosis of a new order of eutherian mammals. Bulletin of the American Museum of Natural History 220:1–214.Google Scholar
Maddison, W. P., and Maddison, D. R. 1992. MacClade: analysis of phylogeny and character evolution, Version 3. Sinauer, Sunderland, Mass.Google Scholar
McKenna, M. C., and Bell, S. K. 1997. Classification of mammals above the species level. Columbia University Press, New York.Google Scholar
Messenger, S. L., and McGuire, J. A. 1998. Morphology, molecules, and the phylogenetics of cetaceans. Systematic Biology 47:90–124.CrossRefGoogle ScholarPubMed
Milinkovitch, M. C., Bérubé, M., and Palsbøll, P. J. 1998. Cetaceans are highly derived artiodactyls. Pp. 113–131in Thewissen, 1998.Google Scholar
Norell, M. A. 1992. Taxic origin and temporal diversity: the effect of phylogeny. Pp. 89–118in Novacek, M. J. and Wheeler, Q. D., eds. Extinction and phylogeny. Columbia University Press, New York.Google Scholar
Norell, M. A., and Novacek, M. J. 1992. The fossil record and evolution: comparing cladistic and paleontologic evidence for vertebrate history. Science 255:1690–1693.CrossRefGoogle ScholarPubMed
Novacek, M. J. 1977. Aspects of the problem of variation, origin and evolution of the eutherian bulla. Mammal Review 7:131–149.CrossRefGoogle Scholar
Novacek, M. J. 1986. The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bulletin of the American Museum of Natural History 183:1–111.Google Scholar
Novacek, M. J. 1992. Fossils, topologies, missing data, and the higher level phylogeny of eutherian mammals. Systematic Biology 41:58–73.CrossRefGoogle Scholar
Novacek, M. J., Gao, K., Norell, M. A., and Rougier, G. A. 1998. Ghost lineages, phylogeny, and ranges of selected vertebrate lineages across the K/T boundary. Journal of Vertebrate Paleontology 18(Suppl. to No. 3):67A.Google Scholar
O'Leary, M. A. 1998. Phylogenetic and morphometric reassessment of the dental evidence for a mesonychian and cetacean clade. Pp. 133–161in Thewissen, 1998.Google Scholar
O'Leary, M. A. 1999a. Whale origins. Science. 283:1641–1642.CrossRefGoogle Scholar
O'Leary, M. A. 1999b. Parsimony analysis of total evidence from extinct and extant taxa, and the cetacean-artiodactyl question (Mammalia, Ungulata). Cladistics 15:315–330.Google ScholarPubMed
O'Leary, M. A., and Geisler, J. H. 1999. The position of Cetacea within Mammalia: Phylogenetic analysis of morphological data from extinct and extant taxa. Systematic Biology 48:455–490.CrossRefGoogle ScholarPubMed
O'Leary, M. A., and Rose, K. D. 1995. Postcranial skeleton of the early Eocene mesonychid Pachyaena (Mammalia: Mesonychia). Journal of Vertebrate Paleontology 15:401–430.CrossRefGoogle Scholar
Prothero, D. R., Manning, E. M., and Fischer, M. 1988. The phylogeny of the ungulates. In Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 2. Mammals. Systematics Association Special Volume 35B:201–234. Clarendon, Oxford.Google Scholar
Sankoff, D., and Rousseau, P. 1975. Locating the vertices of a Steiner tree in arbitrary space. Mathematical Progress 9:240–246.CrossRefGoogle Scholar
Schaeffer, B. 1947. The origin of a mammalian ordinal character. Evolution 2:164–175.CrossRefGoogle Scholar
Shimamura, M., Yasua, H., Ohshmia, K., Abe, H., Kato, H., Kishiro, T., Gotos, M., Munechikai, I., and Okada, N. 1997. Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 388:666–670.CrossRefGoogle Scholar
Shoshani, J. 1986. Mammalian phylogeny: comparison of morphological and molecular results. Molecular Biology and Evolution 3:222–242.Google ScholarPubMed
Siddall, M. E. 1995. Stratigraphic consistency and the shape of things. Systematic Biology 45:111–115.CrossRefGoogle Scholar
Siddall, M. E. 1997. Stratigraphic indices in the balance: a reply to Hitchin and Benton. Systematic Biology 46:569–573.CrossRefGoogle Scholar
Siddall, M. E. 1998. Stratigraphic fit to phylogenies: a proposed solution. Cladistics 14:201–208.Google ScholarPubMed
Slijper, E. J. 1936. Die Cetaceen vergleichend-anatomisch und systematisch. Capita zoologica 7:1–590.Google Scholar
Swift, C. C., and Barnes, L.G. 1996. Stomach contents of Basilosaurus cetoides: implications for the evolution of cetacean feeding behavior, and evidence for vertebrate fauna of epicontinental seas. Paleontological Society Special Publication 8:380.Google Scholar
Swofford, D. L. 1998. “PAUP* 4.0b1: Phylogenetic Analysis Using Parsimony (* and Other Methods).” Sinauer, Sunderland, Mass.Google Scholar
Thewissen, J. G. M. 1994. Phylogenetic aspects of cetacean origins: a morphological perspective. Journal of Mammalian Evolution 2:157–184.CrossRefGoogle Scholar
Thewissen, J. G. M., ed. 1998. The emergence of whales: evolutionary patterns in the origin of Cetacea. Plenum, New York.CrossRefGoogle Scholar
Thewissen, J. G. M., and Domning, D. P. 1992. The role of phenacodontids in the origin of the modern orders of ungulate mammals. Journal of Vertebrate Paleontology 12:494–504.CrossRefGoogle Scholar
Thewissen, J. G. M., and Fish, F. E. 1997. Locomotor evolution in the earliest cetaceans: functional model, modern analogues, and paleontological evidence. Paleobiology 23:482–490.CrossRefGoogle Scholar
Thewissen, J. G. M., and Hussain, S. T. 1993. Origin of underwater hearing in whales. Nature 361:444–445.CrossRefGoogle ScholarPubMed
Thewissen, J. G. M., and Hussain, S. T. 1998. Systematic review of the Pakicetidae, early and middle Eocene Cetacea (Mammalia) from Pakistan and India. Bulletin of the Carnegie Museum of Natural History 34:220–238.Google Scholar
Thewissen, J. G. M., Hussain, S. T., and Arif, M. 1994. Fossil evidence for the origin of aquatic locomotion in archaeocete whales. Science 263:210–212.CrossRefGoogle ScholarPubMed
Thewissen, J. G. M., Madar, S. I., and Hussain, S. T. 1996. Ambulocetus natans, an Eocene cetacean (Mammalia) from Pakistan. Courier Forschungsinstut Senckenberg 191:1–86.Google Scholar
Uhen, M. D. 1996. Dorudon atrox (Mammalia, Cetacea): form, function, and phylogenetic relationships of an archaeocete from the late middle Eocene of Egypt. . University of Michigan, Ann Arbor.Google Scholar
Uhen, M. D. 1998a. Middle to late Eocene basilosaurines and dorudontines. Pp. 29–61in Thewissen, 1998.Google Scholar
Uhen, M. D. 1998b. North American Protocetidae (Cetacea, Archaeoceti). Journal of Vertebrate Paleontology 18(Suppl. to No. 3):83A.Google Scholar
Wagner, P. J. 1995. Stratigraphic tests of cladistic hypotheses. Paleobiology. 21:153–178.CrossRefGoogle Scholar
Webb, S. B., and Taylor, B. E. 1980. Phylogeny of hornless ruminants and a description of the cranium of Archaeomeryx. Bulletin of the American Museum of Natural History 167:1–157.Google Scholar
Wible, J. R. 1987. The eutherian stapedial artery: character analysis and implications for superordinal relationships. Zoological Journal of the Linnaean Society 91:107–135.CrossRefGoogle Scholar
Wible, J. R. 1990. Petrosals of Late Cretaceous marsupials from North America, and a cladistic analysis of the petrosal in therian mammals. Journal of Vertebrate Paleontology 10:183–205.CrossRefGoogle Scholar
Williams, E. M. 1998. Synopsis of the earliest cetaceans: Pakicetidae, Ambulocetidae, Remingtonocetidae, and Protocetidae. Pp. 1–28in Thewissen, 1998.Google Scholar
Witmer, L. M. 1995. The Extant Phylogenetic Bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Woodburne, M. O., and Swisher, C. C. 1995. Land mammal high-resolution geochronology, intercontinental overland dispersals, sea level change, and vicariance. Society for Sedimentary Geology Special Publication 54:335–364.Google Scholar
Zhou, X., Zhai, R., Gingerich, P. D., and Chen, L. 1995. Skull of a new mesonychid (Mammalia, Mesonychia) from the late Paleocene of China. Journal of Vertebrate Paleontology 15:387–400.CrossRefGoogle Scholar