Abstract
Paleostratigraphic estimates of divergence time for nine independent cladogenic events within Mammalia, ranging from 14 to 130 million years, were regressed against Tamura–Nei-corrected 12S rRNA transversions. Relative rate-adjusted distances were also regressed against paleostratigraphic divergence times. The resulting equations were used to estimate interordinal divergence times within Eutheria and Metatheria for a data set that includes representatives of all orders in each infraclass. Without the adjustment for rate variation, divergence times range from 34 to 156 million years for placental orders, versus 32 to 86 million years for marsupial orders. With rate adjustments, the range of divergence estimates decreases to 53 to 133 million years for placentals versus 40 to 79 million years for marsupials. The effect of rate adjustments is most noticeable for carnivores and perissodactyls, where rates are slow, and proboscideans, where rates are fast. In agreement with studies based on nuclear genes, both unadjusted and rate-adjusted estimates of sequence divergence indicate that the majority of placental orders originated before the terminal Cretaceous extinction. Exceptions include the perissodactyl–carnivore split and cladogenesis among paenungulate orders. Most marsupial orders, in turn, may have originated in the early Tertiary although didelphimorphs, at least, appear to have split from other lineages in the late Cretaceous. Marsupial divergence times based on 12S rRNA data are in good agreement with estimates based on single-copy DNA hybridization and disagree with the suggestion of Hershkovitz (1992) that Dromiciops separated from other marsupials in the Jurassic.
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LITERATURE CITED
Allard, M. W., and Miyamoto, M. M. (1992). Testing phylogenetic approaches with empirical data as illustrated with the parsimony method. Mol. Biol. Evol. 9: 778–786.
Anderson, S., Bankie, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R., and Young, I. G. (1981). Sequence and organization of the human mitochondrial genome. Nature 290: 457–465.
Anderson, S., de Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F., and Young, I. G. (1982). Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J. Mol. Biol. 156: 683–717.
Archer, M., Hand, S., and Godthelp, H. (1991). Riversleigh, Reed Books, New South Wales, Australia.
Archibald, J. D. (1996). Fossil evidence for a Late Cretaceous origin of “hoofed” mammals. Science 272: 1150–1153.
Arnason, U., and Gullberg, A. (1993). Comparison between the complete mtDNA sequences of the blue and the fin whale, two species that can hybridize in nature. J. Mol. Evol. 37: 312–322.
Arnason, U., and Johnsson, E. (1992). The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J. Mol. Evol. 34: 493–505.
Arnason, U., Gullberg, A., and Widegren, B. (1991). The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J. Mol. Evol. 33: 556–568.
Arnason, U., Gullberg, A., Johnsson, E., and Ledje, C. (1993). The nucleotide sequence of the mitochondrial DNA molecule of the grey seal, Halichoerus grypus, and a comparison with mitochondrial sequences of other true seals. J. Mol. Evol. 37: 323–330.
Arnason, U., Gullberg, A., Janke, A., and Xu, X. (1996). Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs. J. Mol. Evol. 43: 650–661.
Arnason, U., Gullberg, A., and Janke, A. (1997). Phylogenetic analyses of mitochondrial DNA suggest a sister group relationship between Xenarthra (Edentata) and Ferungulates. Mol. Biol. Evol. 14: 762–768.
Cao, Y., Adachi, J., Yano, T., and Hasegawa, M. (1994). Phylogenetic place of guinea pigs: No support of the rodent-polyphyly hypothesis from maximum-likelihood analyses of multiple protein sequences. Mol. Biol. Evol. 11: 593–604.
Carroll, R. L. (1988). Vertebrate Paleontology and Evolution, Freeman, New York.
Chevret, P. (1994). Etude evolutive des Murinae (Rongeurs: Mammifères) africains par hybridation ADN/ADN. Comparaison avec les approches morphologiques et paleontologiques, Ph.D. thesis, Université Montpellier II, Montpellier, France.
Cooper, A., and Penny, D. (1997). Mass survival of birds across the Cretaceous-Tertiary boundary: Molecular evidence. Science 275: 1109–1113.
D'Erchia, A. M., Gissi, C., Pesole, G., Saccone, C., and Arnason, U. (1996). The guinea-pig is not a rodent. Nature 381: 597–599.
Douzery, E. (1993). Evolutionary relationships among Cetacea based on the sequence of the mitochondrial 12S rRNA gene: Possible paraphyly of toothed-whales (odontocetes) and long separate evolution of sperm whales (Physeteridae). C.R. Acad. Sci. Paris (Ser. II) 316: 1511–1518.
Douzery, E., and Catzeflis, F. M. (1995). Molecular evolution of the mitochondrial 12S rRNA in Ungulata (Mammalia). J. Mol. Evol. 41: 622–636.
Frye, M. S., and Hedges, S. B. (1995). Monophyly of the order Rodentia inferred from mitochondrial DNA sequences of the genes for 12S rRNA, 16S rRNA, and tRNA-valine. Mol. Biol. Evol. 12: 168–176.
Gadaleta, G., Pepe, G., De Candia, G., Quagliariello, C., Sbisa, E., and Saccone, C. (1989). The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: Cryptic signals revealed by comparative analysis between vertebrates. J. Mol. Evol. 28: 497–516.
Garland, T. J., Dickerman, A. W., Janis, C. M., and Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42: 265–292.
Gayet, M., Marshall, L. G., and Sempere, T. (1991). The Mesozoic and Paleocene vertebrates of Bolivia and their stratigraphic context: A review. Revista Tecnica YPFB 12: 393–433.
Gingerich, P. D., Raza, S. M., Arif, M., and Zhou, X. Y. (1994). New whale from the Eocene of Pakistan and the origin of cetacean swimming. Nature 368: 844–847.
Graur, D., Hide, W. A., and Li, W.-H. (1991). Is the guinea-pig a rodent? Nature 351: 649–652.
Graur, D., Gouy, M., and Duret, L. (1997). Evolutionary affinities of the order Perissodactyla and the phylogenetic status of the superordinal taxa Ungulata and Altungulata. Mol. Phylogenet. Evol. 7: 195–200.
Hanni, C., Laudet, V., Barriel, V., and Catzeflis, F. M. (1995). Evolutionary relationships of Acomys and other murids (Rodentia, Mammalia) based on complete 12S rRNA mitochondrial gene sequences. Israel J. Zool. 41: 131–146.
Hartenberger, J.-L. (1994). The evolution of the Gliroidea. In: Rodent and Lagomorph Families of Asian Origins and Diversification, Y. Tomida, C. K. Li, and T. Setoguchi, eds., pp. 19–33, National Science Museum Monographs, Number 8, Tokyo.
Hedges, S. B., Parker, P. H., Sibley, C. G., and Kumar, S. (1996). Continental breakup and the ordinal diversification of birds and mammals. Nature 381: 226–229.
Hershkovitz, P. (1992). Ankle bones: The Chilean opossum Dromiciops gliroides Thomas, and marsupial phylogeny. Bonn. Zool. Beitr. 43: 181–213.
Hillis, D. M., Mable, B. K., and Moritz, C. (1996). Applications of molecular systematics. In: Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Mable, eds., pp. 515–543, Sinauer, Sunderland, MA.
Hixson, J. E., and Brown, W. M. (1986). A comparison of the small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: Sequence, structure, evolution, and phylogenetic implications. Mol. Biol. Evol. 3: 1–18.
Hollar, L. J., and Springer, M. S. (1997). Old world fruitbat phylogeny: Evidence for convergent evolution and an endemic African clade. Proc. Natl. Acad. Sci. USA 94: 5716–5721.
Hope, R., Cooper, S., and Wainwright, B. (1990). Globin macromolecular sequences in marsupials and monotremes. In: Mammals from Pouches and Eggs: Genetics, Breeding, and Evolution of Marsupials and Monotremes, J. A. Marshall Greves, R. M. Hope, and D. W. Cooper, eds., pp. 147–171, CSIRO, Melbourne, Australia.
Janke, A., Xu, X., and Arnason, U. (1997). The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. Proc. Natl. Acad. Sci. USA 94: 1276–1281.
Janke, A., Feldmaier-Fuchs, G., Thomas, W. K., von Haeseler, A., and Paabo, S. (1994). The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137: 243–256.
Kirsch, J. A. W., Lapointe, F.-J., and Springer, M. S. (1997). DNA-hybridization studies of marsupials and their implications for metatherian classification. Aust. J. Zool. 45: 211–280.
Kishino, H., and Hasegawa, M. (1989). Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29: 170–179.
Krajewski, C., Blacket, M., Buckley, L., and Westerman, M. (1997). A multigene assessment of phylogenetic relationships within the dasyurid marsupial subfamily Sminthopsinae. Mol. Phylogenet. Evol. 8: 236–248.
Kraus, F., and Miyamoto, M. M. (1991). Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst. Zool. 40: 117–130.
Krettek, A., Gullberg, A., and Arnason, U. (1995). Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J. Mol. Evol. 41: 952–957.
Lavergne, A., Douzery, E., Stichler, T., Catzeflis, F. M., and Springer, M. S. (1996). Interordinal mammalian relationships: evidence for paenungulate monophyly is provided by complete mitochondrial 12S rRNA sequences. Mol. Phylogenet. Evol. 6: 245–258.
Li, W.-H., Hide, W. A., Zharkikh, A., Ma, D.-P., and Graur, D. (1992). The molecular taxonomy and evolution of the guinea pig. J. Hered. 83: 174–181.
Lopez, J. V., Cevario, S., and O'Brien, S. J. (1996). Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33: 229–246.
Luckett, W. P., and Hartenberger, J.-L. (1993). Monophyly or polyphyly of the Order Rodentia: Possible conflict between morphological and molecular interpretations. J. Mammal. Evol. 1: 127–147.
MacPhee, R. D. E., and Novacek, M. J. (1993). Definition and relationships of Lipotyphla. In: Mammal Phylogeny, 2. Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 13–31, Springer, New York.
Madsen, O., Deen, P. M. T., Pesole, G., Saccone, C., and de Jong, W. W. (1997). Molecular evolution of mammalian aquaporin-2: Further evidence that elephant shrew and aardvark join the paenungulate clade. Mol. Biol. Evol. 14: 363–371.
Marshall, C. R. (1990a). The fossil record and estimating divergence times between lineages: Maximum divergence times and the importance of reliable phylogenies. J. Mol. Evol. 30: 400–4081.
Marshall, C. R. (1990b). Confidence intervals on stratigraphic ranges. Paleobiology 16: 1–10.
Martin, A. P., and Palumbi, S. R. (1993). Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl. Acad. Sci. USA 90: 4087–4091.
Miyamoto, M. M., and Goodman, M. (1986). Biomolecular systematics of eutherian mammals: Phylogenetic patterns and classification. Syst. Zool. 35: 230–240.
Miyamoto, M. M., Kraus, F., and Ryder, O. A. (1990). Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc. Natl. Acad. Sci. USA 87: 6127–6131.
Novacek, M. J. (1992). Mammalian phylogeny: Shaking the tree. Nature 356: 121–125.
Novacek, M. J. (1993). Reflections on higher mammalian phylogenetics. J. Mammal. Evol. 1: 3–30.
Porter, C. A., Goodman, M., and Stanhope, M. J. (1996). Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand factor gene. Mol. Phylogenet. Evol. 5: 89–101.
Rich, T. H., Vickers-Rich, P., Constantine, A., Flannery, T. F., Kool, L. and van Klaveren, N. (1997). A tribosphenic mammal from the Mesozoic of Australia. Science 278: 1438–1442.
Richardson, B. J. (1988). A new view on the relationships of Australian and American marsupials. Austral. Mammal. 11: 71–73.
Romer, A. S. (1966). Vertebrate Paleontology, University of Chicago Press, Chicago.
Sourrouille, P., Hanni, C., Ruedi, M., and Catzeflis, F. (1995). Molecular systematics of Mus crociduroides, an endemic mouse of Sumatra (Muridae: Rodentia). Mammalia 59: 91–102.
Springer, M. S. (1995). Molecular clocks and the incompleteness of the fossil record. J. Mol. Evol. 41: 531–538.
Springer, M. S., and Douzery, E. (1996). Secondary structure, conservation of functional sites, and rates of evolution among mammalian mitochondrial 12S rRNA genes based on sequences from placentals, marsupials, and a monotreme. J. Mol. Evol. 43: 357–373.
Springer, M. S., and Kirsch, J. A. W. (1991). DNA hybridization, the compression effect, and the radiation of diprotodontian marsupials. Syst. Zool. 40: 131–151.
Springer, M., and Lilje, A. (1988). Gap analysis and biostratigraphy: the expected sequence of biostratigraphic events. J. Geol. 96: 228–236.
Springer, M. S., Westerman, M., and Kirsch, J. A. W. (1994). Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation. J. Mammal. Evol. 2: 85–115.
Springer, M. S., Hollar, L. J., and Burk, A. (1995). Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol. Biol. Evol. 12: 1138–1150.
Springer, M. S., Burk, A., Kavanagh, J. R., Waddell, V. G., and Stanhope, M. J. (1997a). The interphotoreceptor retinoid binding protein gene in therian mammals: Implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc. Natl. Acad. Sci. USA 94: 13754–13759.
Springer, M. S., Cleven, G. C., Madsen, O., de Jong, W. W., Waddell, V. G., Amrine, H. M., and Stanhope, M. J. (1997b). Endemic African mammals shake the phylogenetic tree. Nature 388: 61–64.
Springer, M. S., Kirsch, J. A. W., and Case, J. A. (1997c). The chronicle of marsupial evolution. In: Molecular Evolution and Adaptive Radiations, T. Givnish and K. Sytsma, eds., Cambridge University Press, Cambridge.
Stanhope, M. J., Smith, M. R., Waddell, V. G., Porter, C. A., Shivji, M. S., and Goodman, M. (1996). Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: Convincing evidence for several superordinal clades. J. Mol. Evol. 43: 83–92.
Strauss, D., and Sadler, P. M. (1989). Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Math. Geol. 21: 411–427.
Sullivan, J., and Swofford, D. L. (1997). Are guinea pigs rodents? The importance of adequate models in molecular phylogenetics. J. Mammal. Evol. 4: 77–86.
Swofford, D. L., Olsen, G. J., Waddell, P. J., and Hillis, D. M. (1996). Phylogenetic inference. In: Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Mable, eds., Sinauer, Sunderland, MA.
Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512–526.
Tanhauser, S. (1985). Evolution of Mitochondrial DNA: Patterns and Rate of Change, Ph.D. dissertation. University of Florida, Gainesville.
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.
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.
Wilson, A. C., Ochman, H., and Prager, E. M. (1987). Molecular time scale for evolution. Trends Genet. 3: 241–247.
Xu, X., and Arnason, U. (1994). The complete mitochondrial DNA sequence of the horse, Equus caballus: Extensive heteroplasmy of the control region. Gene 148: 357–362.
Zar, J. H. (1984). Biostatistical Analysis, Prentice-Hall, Englewood Cliffs, NJ.
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Springer, M.S. Molecular Clocks and the Timing of the Placental and Marsupial Radiations in Relation to the Cretaceous–Tertiary Boundary. Journal of Mammalian Evolution 4, 285–302 (1997). https://doi.org/10.1023/A:1027378615412
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DOI: https://doi.org/10.1023/A:1027378615412