Skip to main content
SpringerLink
Log in

MtDNA Evidence for Repeated Pulses of Speciation Within Arvicoline and Murid Rodents

  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

We examined temporal aspects of phylogenetic relationships among 5 murid rodent subfamilies and 11 arvicoline genera based on DNA sequences of the cytochrome b gene (n = 92) and ND4 gene (n = 17). We found monophyly for Muridae but a polytomy among murid subfamilies. Arvicolinae was monophyletic, but most genera within this subfamily arose from a polytomy. Microtus was monophyletic, but within the genus, species arose rapidly. This pattern of nested pulses (polytomies) was recovered across parsimony, distance, and likelihood methods and indicates that accumulation of taxonomic diversity in murids was sporadic, rather than gradual. Arvicolines appeared in the Late Miocene and diversified later, between 3 and 5 million years ago. A relatively high rate of sequence evolution (i.e., 2.3% in third-position transversions per million years) helps reconcile the diversification of fossils and mtDNA lineages.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

LITERATURE CITED

  • Alston, E. R. (1876). On the classification of the Order Glires. Proc. Zool. Soc. London 1876: 61–98.

    Google Scholar 

  • Anderson, S. (1974). Patterns of faunal evolution. Q. Rev. Biol. 49: 311–332.

    Google Scholar 

  • Arévalo, E., Davis, S. K., and Sites, J. W., Jr. (1994). Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst. Biol. 43: 387–418.

    Google Scholar 

  • Bailey, V. (1990). Revision of the American voles of the genus Microtus. North Am. Fauna 17: 1–88.

    Google Scholar 

  • Baker, R. J., Van Den Bussche, R. A., Wright, A. J., Wiggins, L. E., Hamilton, M. J., Reat, E. P., Smith, M. H., Lomakin, M. D., and Chesser, R. K. (1996). High levels of genetic change in rodents of Chernobyl. Nature 380: 801–802.

    Google Scholar 

  • Barnosky, A. D. (1987). Punctuated equilibrium and phyletic gradualism. In: Current Mammalogy, Vol. 1, H. H. Genoways, ed., pp. 109–147, Plenum Press, New York.

    Google Scholar 

  • Bennett, K. D. (1990). Milankovitch cycles and their effects on species in ecological and evolutionary time. Paleobiology 16: 11–21.

    Google Scholar 

  • Bibb, M. J., Van Etten, R. A., Wright, C. T., Walberg, N. W., and Clayton, D. A. (1981). Sequence and gene organization of mouse mitochondrial DNA. Cell 26: 167–180.

    Google Scholar 

  • Bremer, K. (1988). The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42: 795–803.

    Google Scholar 

  • Carleton, M. D. (1985). Macroanatomy. In: Biology of New World Microtus, R. H. Tamarin, ed., pp. 116–175, Special Publication, American Society of Mammalogists.

  • Carleton, M. D., and Musser, G. G. (1984). Muroid rodents. In: Order and Families of Recent Mammals of the World, S. Anderson and J. K. Jones, Jr., eds., pp. 289–379, John Wiley & Sons, New York.

    Google Scholar 

  • Catzeflis, F. M., Nevo, E., Ahlquist, J. E., and Sibley, C. G. (1989). Relationships of the chromosomal species in the Eurasian mole rats of the Spalax ehrenbergi group as determined by DNA-DNA hybridization, and an estimate of the spalacid-murid divergence time. J. Mol. Evol. 29: 223–232.

    Google Scholar 

  • Catzeflis, F. M., Aguilar, J.-P., and Jaeger, J.-J. (1992). Muroid rodents: Phylogeny and evolution. TREE 7: 122–126.

    Google Scholar 

  • Catzeflis, F. M., Hänni, C., Sourrouille, P., and Douzery, E. (1995). Re: Molecular systematics of hystricognath rodents: The contribution of sciurognath mitochondrial 12S rRNA sequences. Mol. Phyl. Evol. 4: 357–360.

    Google Scholar 

  • Chaline, J. (1987). Arvicolid data (Arvicolidae, Rodentia) and evolutionary concepts. In: Evolutionary Biology, Vol. 21, M. K. Hecht, B. Wallace, and G. T. Prance, eds., pp. 237–310, Plenum Press, New York.

    Google Scholar 

  • Chaline, J. (1990). An approach to studies of fossil arvicolids. In: International Symposium on Evolutionary Phylogenetics and Biostratigraphy of Arvicolids, O. Fejfar and W. Heinrich, eds., pp. 45–84, Pfeil-Verlag, Prague.

    Google Scholar 

  • Chaline, J., and Graf, J.-D. (1988). Phylogeny of the Arvicolidae (Rodentia): Biochemical and paleontological evidence. J. Mammal. 69: 22–33.

    Google Scholar 

  • Chaline, J., Laurin, B., Brunet-Lecomte, P., and Viriot, L. (1993). Morphological trends and rates of evolution in arvicolids (Arvicolidae, Rodentia): Towards a punctuated equilibrium/disequlibrium model. Quaternary Int. 19: 27–39.

    Google Scholar 

  • Chippendale, P. T., and Weins, J. J. (1994). Weighting, partitioning, and combining characters in phylogenetic analysis. Syst. Biol. 43: 278–287.

    Google Scholar 

  • Conroy, C. J., and Cook, J. A. (1999). Molecular systematics of a holarctic rodent (Microtus: Muridae). J. Mammal. (in press).

  • Cooper, A., and Fortey, R. (1998). Evolutionary explosions and the phylogenetic fuse. TREE 13: 151–156.

    Google Scholar 

  • Courant, F., David, B., Laurin, B., and Chaline, J. (1997). Quantification of cranial convergences in arvicolids (Rodentia). Biol. J. Linn. Soc. 62: 505–517.

    Google Scholar 

  • DeBry, R. W. (1992). Biogeography of New World taiga-dwelling Microtus (Mammalia: Arvicolidae): A hypothesis test that accounts for phylogenetic uncertainty. Evolution 46: 1347–1357.

    Google Scholar 

  • Engel, S. R., Hogan, K. M., Taylor, J. F., and Davis, S. K. (1998). Molecular systematics and paleobiogeography of the South American sigmodontine rodents. Mol. Biol. Evol. 15: 35–49.

    Google Scholar 

  • Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package), Version 3.57c, University of Washington, Seattle.

    Google Scholar 

  • Flynn, L. J., Jacobs, L. L., and Lindsay, E. H. (1985). Problems in muroid phylogeny: Relationship to other rodents and origin of major groups. In: Evolutionary Relationships Among Rodents: A Multidisciplinary Analysis, W. P. Luckett and J.-L. Hartenberger, eds., pp. 589–616, Plenum Press, New York.

    Google Scholar 

  • Gilëva, E. A., Rybnikov, D. E., and Miroshnichenko, G. P. (1990). DNA-DNA hybridization and phylogenetic relationships in two genera of voles, Alticola and Clethrionomys (Microtinae: Rodentia). Doklady Nauk SSSR 311: 477–480.

    Google Scholar 

  • Givnish, T. J., and Sytsma, K. J. (eds.) (1997). Molecular Evolution and Adaptive Radiation, Cambridge University Press, Cambridge and New York.

    Google Scholar 

  • Gromov, I. M., and Polyakov, I. Ya. (1977). Fauna SSSR, Mlekopitayushchie, tom 3, vyp. 8 [Fauna of the USSR, Vol. 3, Part 8. Mammals]. Polevki [Voles (Microtinae)]. Nauka, Moscow-Leningrad. (English translation, Smithsonian Institution, Washington, DC.)

    Google Scholar 

  • Hillis, D. M., and Huelsenbeck, J. P. (1992). Signal, noise, and reliability in molecular phylogenetic analyses. J. Hered. 83: 189–195.

    Google Scholar 

  • Hillis, D. M., Moritz, C., and Mable, B. K. (1996). Applications of molecular systematics. In: Molecular Systematis, 2nd ed., D. M. Hillis, C. Moritz, and B. K. Mable, eds., pp. pp. 515–544, Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Hinton, M. A. C. (1926). Monograph of the Voles and Lemmings (Microtinae) Living and Extinct, Vol. 1, Trust. Br. Mus., London.

    Google Scholar 

  • Hoffmann, R. S. and Koeppl, J. W. (1985). Zoogeography. In: Biology of New World Microtus, R. H. Tamarin, ed., pp. 84–115, Special Publication, American Society of Mammalogists.

  • Hooper, E. T., and Hart, B. S. (1962). A synopsis of Recent North American microtine rodents. Misc. Publ. Mus. Zool. Univ. Mich. 120: 1–68.

    Google Scholar 

  • Huelsenbeck, J. P., Swofford, D. L., Cunningham, C. W., Bull, J. J., and Waddell, P. J. (1994). Is character weighting a panacea for the problem of data heterogeneity in phylogenetic analysis? Syst. Biol. 43: 288–291.

    Google Scholar 

  • Huston, M. A. (1995). Biological Diversity: The Coexistence of Species on Changing Landscapes, Cambridge University Press, Cambridge.

    Google Scholar 

  • Irwin, D. M., Kocher, T. D., and Wilson, A. C. (1991). Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128–144.

    Google Scholar 

  • Jarrell, G. H., and Fredga, K. (1993). How many kinds of lemmings? In: The Biology of Lemmings, pp. 45–57, Linnean Society of London, London.

    Google Scholar 

  • Jermiin, L. S., Graur, D., Lowe, R. M., and Crozier, R. H. (1994). Analysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes. J. Mol. Evol. 39: 160–173.

    Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative study of nucleotide sequences. J. Mol. Evol. 16: 111–120.

    Google Scholar 

  • 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.

    Google Scholar 

  • Kitching, I. J. (1994). The determination of character polarity. In: Cladistics: A Practical Course in Systematics, P. L. Forey, C. J. Humphries, I. J. Kitching, R. W. Scotland, D. J. Siebert, and D. M. Williams, eds., pp. 22–43, Oxford Science, Systematics Association Publication No. 10, Oxford.

  • Klicka, J., and Zink, R. M. (1997). The importance of recent ice ages in speciation: A failed paradigm. Science 277: 1666–1669.

    Google Scholar 

  • Kraus, F., and Miyamoto, M. M. (1991). Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst. Zool. 40: 117–130.

    Google Scholar 

  • Kumar, S., Tamura, K., and Nei, M. (1993). MEGA: Molecular Evolutionary Genetics Analysis, Version 1.02, Pennsylvania State University, University Park.

    Google Scholar 

  • Lara, M. C., Patton, J. L., and Da Silva, M. N. F. (1996). The simultaneous diversification of South American echimyid rodents (Hystricognathi) based on complete cytochrome b sequences. Mol. Phyl. Evol. 5: 403–413.

    Google Scholar 

  • Lessa, E. P., and Cook, J. A. (1998). The molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation. Mol. Phyl. Evol. 9: 88–99.

    Google Scholar 

  • Maddison, D. R. (1991). The discovery and importance of multiple islands of most-parsimonious trees. Syst. Zool. 40: 315–328.

    Google Scholar 

  • Maddison, W. P., and Maddison, D. R. (1992). MacClade 3.0: Interactive Analysis of Phylogeney and Character Evolution, Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • 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.

    Google Scholar 

  • Martin, L. D. (1975). Microtine rodents from the Ogallala Pliocene of Nebraska and the early evolution of the Microtinae in North America. Univ. Mich. Pap. Paleontol. 12: 101–110.

    Google Scholar 

  • Matthey, R. (1957). Cytolgie comparée, systématique et phylogénie des Microtinae (Rodentia-Muridae). Rev. Suisse Zool. 64: 39–71.

    Google Scholar 

  • Medrano, J. F., Aasen, E., and Sparrow, L. (1990). DNA extraction from nucleated red blood cells. Biotechniques 8: 43.

    Google Scholar 

  • Miller, G. S., Jr. (1896). The genera and subgenera of voles and lemmings. North Am. Fauna 12: 1–84.

    Google Scholar 

  • Modi, W. S. (1987). Phylogenetic analyses of the chromosomal banding patterns among the Nearctic Arvicolidae. Syst. Zool. 36: 109–136.

    Google Scholar 

  • Modi, W. S. (1996). Phylogenetic history of LINE-1 among arvicolid rodents. Mol. Biol. Evol. 13: 633–641.

    Google Scholar 

  • Mooers, A. Ø., and Heard, S. B. (1997). Inferring evolutionary process from phylogenetic tree shape. Q. Rev. Biol. 72: 31–54.

    Google Scholar 

  • Musser, G. G., and Carleton, M. D. (1993). Family Muridae. In: Mammal Species of the World: A Taxonomic and Geographic Reference, 2nd ed., D. E. Wilson and D. M. Reeder, eds., pp. 501–755, Smithsonian Institution Press, Washington, DC, and London.

    Google Scholar 

  • Nadler, C. F., Zhurkevich, N. M., Hoffmann, R. S. Kozlovskii, A. I., Deutsch, L., and Nadler, C. F., Jr. (1978). Biochemical relationships of the Holarctic vole genera (Clethrionomys, Microtus, and Arvicola (Rodentia: Arvicolinae)). Can. J. Zool. 56: 1564–1575.

    Google Scholar 

  • Naylor, G. J. P., and Brown, W. M. (1998). Amphioxus mitochondrial DNA, chordate phylogeny, and the limits of inference based on comparisons of sequences. Syst. Biol. 47: 61–76.

    Google Scholar 

  • Nikoletopoulos, N. P., Chondropoulos, B. P., and Fraguedakis-Tsolis, S. E. (1992). Albumin evolution and phylogenetic relationships among Greek rodents of the families Arvicolidae and Muridae. J. Zool. Lond. 228: 445–453.

    Google Scholar 

  • Novacek, M. J. (1992). Fossils, topologies, missing data, and the higher level phylogeny of eutherian mammals. Syst. Biol. 41: 58–73.

    Google Scholar 

  • O'hUigin, C., and Li, W.-H. (1992). The molecular clock ticks regularly in muroid rodents and hamsters. J. Mol. Evol. 35: 377–384.

    Google Scholar 

  • Patton, J. L., dos Reis, S. F., and da Silva, M. N. F. (1996). Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome b gene. J. Mammal. Evol. 3: 3–29.

    Google Scholar 

  • Reig, O. A. (1989). Karyotypic repatternings as one triggering factor in cases of explosive speciation. In: Evolutionary Biology of Transient Unstable Populations, A. Fontdevila, ed., pp. 246–289, Springer-Verlag, Berlin.

    Google Scholar 

  • Repenning, C. A. (1968). Mandibular musculature and the origin of the subfamily Arvicolinae (Rodentia). Acta Zool. Cracov 13: 29–72.

    Google Scholar 

  • Repenning, C. A., Fejfar, O., and Heinrich, W.-D. (1990). Arvicolid rodent biochronology of the Northern Hemisphere. In: International Symposium on the Evolution and Phylogenetic Biostratigraphy of Arvicolids, O. Fejfar and W.-D. Heinrich, eds., pp. 385–418, Pfeil-Verlag, Prague.

    Google Scholar 

  • Riddle, B. R. (1995). Molecular biogeography in the pocket mice (Perognathus and Chaetodipus) and grasshopper mice (Onychomys): The late Cenozoic development of a North American aridlands rodent guild. J. Mammal. 76: 283–301.

    Google Scholar 

  • Robinson, M., Catzeflis, F., Briolay, J., and Mouchiroud, D. (1997). Molecular phylogeny of rodents, with special emphasis on murids: Evidence from nuclear gene LCAT. Mol. Phyl. Evol. 8: 423–434.

    Google Scholar 

  • Ruedas, L. A., and Kirsch, J. A. W. (1997). Systematics of Maxomys Sody, 1936 (Rodentia: Muridae: Murinae): DNA/DNA hybridization studies of some Borneo-Javan species and allied Sundaic and Australo-Papuan genera. Biol. J. Linn. Soc. 61: 385–408.

    Google Scholar 

  • Russo, C. A. M., Takezaki, N., and Nei, M. (1996). Efficiencies of different genes and different tree-building methods in recovering a known phylogeny. Mol. Biol. Evol. 13: 525–536.

    Google Scholar 

  • Saiki, R. K., Gefland, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1988). Primer-directed enzymatic amplifications of DNA with thermostable DNA polymerase. Science 239: 487–491.

    Google Scholar 

  • Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    Google Scholar 

  • Sanderson, M. J., and Donoghue, M. J. (1996). Reconstructing shifts in diversification rates on phylogenetic trees. TREE 11: 15–20.

    Google Scholar 

  • Smith, M. F., and Patton, J. L. (1993). The diversification of South American murid rodents: Evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol. J. Linn. Soc. 50: 149–177.

    Google Scholar 

  • Sorenson, M. D. (1996). TreeRot, University of Michigan, Ann Arbor.

    Google Scholar 

  • Springer, M. S. (1995). Molecular clocks and the incompleteness of the fossil record. J. Mol. Evol. 41: 531–538.

    Google Scholar 

  • Stanley, S. M. (1979). Macroevolution: Pattern and Process, W. H. Freeman, San Francisco.

    Google Scholar 

  • Swofford, D. L. (1997). PAUP*4.0d59: Phylogenetic Analysis Using Parsimony, distributed by the author.

  • Tajima, F. (1993). Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135: 599–607.

    Google Scholar 

  • Tan, A.-M., and Wake, D. B. (1995). MtDNA phylogeography of the California newt, Taricha torosa (Caudata, Salamandridae). Mol. Phyl. Evol. 4: 383–394.

    Google Scholar 

  • Vrba, E. S. (1993). Turnover-pulses, the Red Queen, and related topics. Am. J. Sci. 293-A: 418–452.

    Google Scholar 

  • Vrba, E. S. (1995). On the connection between paleoclimate and evolution. In: Paleoclimate and Evolution, with Emphasis on Human Origins, E. S. Vrba, G. H. Denton, T. C. Partridge, and L. H. Burckle, eds., pp. 24–45, Yale University Press, New Haven, CT.

    Google Scholar 

  • Wakeley, J. (1996). The excess of transitions among nucleotide substitutions: New methods of estimating transition bias underscore its significance. TREE 11: 158–163.

    Google Scholar 

  • Wilson, D. E., and Reeder, D. M. (1993). Mammal Species of the World: A Taxonomic and Geographic Reference, 2nd ed., Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Wu, C.-I., and Li, W.-H. (1985). Evidence for higher rates of nucleotide substitutions in rodents than in man. Proc. Natl. Acad. Sci. USA 82: 1741–1745.

    Google Scholar 

  • Zakrzewski, R. J. (1985). The fossil record. In: Biology of New World Microtus, R. H. Tamarin, ed., pp. 1–51, Special Publication No. 8, American Society of Mammalogists.

  • Zardoya, R., and Meyer, A. (1996). Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates. Mol. Biol. Evol. 13: 933–942.

    Google Scholar 

Download references

Author information

Author notes

  1. Chris J. Conroy

    Present address: Department of Biological Sciences, Stanford University, Stanford, California, 94305-5020

Authors and Affiliations

  1. University of Alaska Museum and Institute of Arctic Biology, 907 Yukon Drive, Fairbanks, Alaska, 99775-6960

    Chris J. Conroy & Joseph A. Cook

Authors
  1. Chris J. Conroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph A. Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conroy, C.J., Cook, J.A. MtDNA Evidence for Repeated Pulses of Speciation Within Arvicoline and Murid Rodents. Journal of Mammalian Evolution 6, 221–245 (1999). https://doi.org/10.1023/A:1020561623890

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020561623890

Search

Navigation