Journal of Mammalian Evolution

, Volume 3, Issue 2, pp 97–120 | Cite as

Resolution of recent radiations within three evolutionary lineages of felidae using mitochondrial restriction fragment length polymorphism variation

  • Warren E. Johnson
  • Peter A. Dratch
  • Janice S. Martenson
  • Stephen J. O'Brien

Abstract

Patterns of mitochondrial restriction fragment length polymorphism (RFLP) variation were used to resolve more recent relationships among the species of the Felidae ocelot lineage, domestic cat lineage, and pantherine lineage. Twenty-five of 28 restriction enzymes revealed site variation in at least 1 of 21 cat species. The ocelot lineage was resolved into three separate sistertaxa groups: Geoffroy's cat (Oncifelis geoffroyi) and kodkod (O. guigna), ocelot (Leopardus pardalis) and margay (L. wiedii), and pampas cat (Lynchailurus colocolo) and most of the tigrina samples (Leopardus tigrina). Within the domestic cat lineage, domestic cat (Felis catus), European wild cat (F. silvestris), and African wild cat (F. libyca) formed a monophyletic trichotomy, which was joined with sand cat (F. margarita) to a common ancestor. Jungle cat (F. chaus) and black-footed cat (F. nigripes) mtDNAs diverged earlier than those of the other domestic cat lineage species and are less closely related. Within the pantherine lineage, phylogenetic analysis identified two distinct groups, uniting lion (P. leo) with leopard (P. pardus) and tiger (P. tigris) with snow leopard (P. uncia).

Key Words

Felidae mitochondrial DNA phylogenetic reconstruction restriction fragment length polymorphism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Avise, J. C. (1991). Ten unorthodox perspectives on evolution prompted by comparative population genetic findings on mitochondrial DNA.Annu. Rev. Genet. 25: 45–69.PubMedGoogle Scholar
  2. Avise, J. C. (1994).Molecular Markers, Natural History and Evolution, Chapman and Hall, New York.Google Scholar
  3. Avise, J. C., Neigel, J. E., and Arnold, J. (1984). Demographic influences of mitochondrial DNA lineage survivorship in animal populations.J. Mol. Evol. 20: 99–105.PubMedGoogle Scholar
  4. Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A., and Saunders, N. C. (1987). Intraspecific phylogeography: The mitochondrial DNA bridge between population genetics and systematics.Annu. Rev. Ecol. Syst. 18: 489–522.Google Scholar
  5. Avise, J. C., Bowen, B. W., Lamb, T., Meylan, A. B., and Bermingham, E. (1992). Mitochondrial DNA evolution at a turtle's pace: Evidence for low genetic variability and reduced microevolutionary rate in the Testudines.Mol. Biol. Evol. 9: 457–473.PubMedGoogle Scholar
  6. Benveniste, R. E. (1985). The contributions of retroviruses to the study of mammalian evolution. In;Molecular Evolutionary Genetics, R. J. Macintyre, ed., pp. 359–417, Plenum Press, New York.Google Scholar
  7. Benveniste, R. E., and Todaro, G. J. (1974). Evolution of C-type viral genes: Inheritance of exogenously acquired viral genes.Nature 252: 456–459.PubMedGoogle Scholar
  8. Benveniste, R. E., Sherr, C. J., and Todaro, G. J. (1975). Evolution of type C viral genes: Origin of feline leukemia virus.Science 190: 886–888.PubMedGoogle Scholar
  9. Berta, A. (1983). A new species of small cat (Felidae) from the late Pliocene-early Pleistocene Uquian of Argentina.J. Mammal. 64: 720–725.Google Scholar
  10. Brown, W. M. (1985). The mitochondrial genome of animals. In:Molecular Evolutionary Genetics, R. J. MacIntyre, ed., pp. 95–130, Plenum Press, New York.Google Scholar
  11. Collier, G. E., and O'Brien, S. J. (1985). A molecular phylogeny of the Felidae: Immunological distance.Evolution 39: 473–487.Google Scholar
  12. Cronin, M. A. (1991). Mitochondrial-DNA phylogeny of deer (Cervidae).J. Mammal. 72: 553–566.Google Scholar
  13. DeBry, R. W., and Slade, N. A. (1985). Cladistic analysis of restiction endonuclease cleavage maps within a maximum-likelihood framework.Gyst. Zool. 34: 21–34.Google Scholar
  14. DeSalle, R., and Templeton, A. R. (1988). Founder effects and the rate of mitochondrial DNA evolution in HawaiianDrosophila.Evolution 42: 1076–1084.Google Scholar
  15. Ewer, R. F. (1973).The Carnivores, Cornell University Press, Ithaca, NY.Google Scholar
  16. Farris, J. S. (1977). Phylogenetic analysis under Dollo's law.Syst. Zool. 26: 77–88.Google Scholar
  17. Felsenstein, J. (1993).PHYLIP, Phylogeny Inference Package (Version 3.5), University of Washington, Seattle.Google Scholar
  18. Ficcarelli, G. (1984). The Villafranchian cheetahs from Tuscany and remarks on the dispersal and evolution of the genusAcinomyx.Palaeontogr. Italica 73: 94–103.Google Scholar
  19. Glass, G. E., and Martin, L. D. (1978). A multivariate comparison of some extant and fossil Felidae.Carnivore 1: 80–87.Google Scholar
  20. Guggisberg, C. A. W. (ed.) (1975).Wild Cats of the World, Taplinger, New York.Google Scholar
  21. Hemmer, H. (1978). The evolutionary systematics of living Felidae: Present status and current problems.Carnivore 1: 71–78.Google Scholar
  22. Herrington, S. J. (1986).Phylogenetic Relationships of the Wild Cats of the World, Ph.D. dissertation, University of Kansas, Lawrence.Google Scholar
  23. Hunt, R. M. (1989). Evolution of the aeluroid Carnivora: Significance of the ventral promontorial process of the petrosal, and the origin of basicranial patterns in the living families.Am. Mus. Novit. 2930; 1–32.Google Scholar
  24. Janczewski, D. N., Modi, W. S., Stephens, J. C., and O'Brien, S. J. (1995). Molecular evolution of mitochondrial 12S RNA and cytochrome b sequences in the pantherine lineage of Felidae.Mol. Biol. Evol. 12: 690–707.PubMedGoogle Scholar
  25. Kurtén, B. (1965). On the evolution of the European wild cat,Felis silvestres Schreber.Acta Zool. Fennica 111: 1–29.Google Scholar
  26. Lopez, J. V., Yuhki, N., Masuda, R., Modi, W., and O'Brien, S. J. (1994).Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat.J. Mol. Evol. 39: 174–190.PubMedGoogle Scholar
  27. 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.PubMedGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. Martin, A. P., Naylor, G. J. P., and Palumbi, S. R. (1992). Rates of mitochondrial DNA evolution in sharks are slow compared with mammals.Nature 357: 153–155.PubMedGoogle Scholar
  30. Martin, L. D. (1989). Fossil history of the terrestrial Carnivora. In:Carnivore Behavior, Ecology and Evolution, J. L. Gittleman, ed., pp. 536–568, Cornell University Press, Ithaca, NY.Google Scholar
  31. Masuda, R., Lopez, J. V., Pecon Slattery, J., Yuhki, N., and O'Brien, S. J. (1996). Molecular phylogeny of mitochondrial 12s rRNA and cytochrome b sequences in the Felidae: Ocelot and domestic cat lineages.Mol. Phylo. Evol. (in press).Google Scholar
  32. Menotti-Raymond, M., and O'Brien, s. J. (1993). Dating the genetic bottleneck of the African cheetah.Proc. Natl. Acad. Sci. USA 90: 3172–3176.PubMedGoogle Scholar
  33. Miththapala, S., Seidensticker, J., and O'Brien, S. J. (1996). Phylogeographic subspecies recognition in the leopards (Panthera pardus): Molecular genetic variation.Conserv. Biol. (in press).Google Scholar
  34. Modi, W. S., and O'Brien, S. J. (1988). Quantitative cladistic analysis of chromosomal banding among species in three orders of mammals: Hominoid primates, felids and arvicolid rodents. In;Chromosome Structure and Function, J. P. Gustafson and R. Appels, eds., pp. 215–242, Plenum Press, New York.Google Scholar
  35. Modi, W. S., Nash, W. G., Ferrari, A. C., and O'Brien, S. J. (1987). Cytogenetic methodologies for gene mapping and comparative analyses in mammalian cell culture systems.Gene Anal. Tech. 4: 75–85.PubMedGoogle Scholar
  36. Moritz, C., Dowling, T. E., and Brown, W. M. (1987). Evolution of animal mitochondrial DNA: Relevance for population biology and systematics.Annu. Rev. Ecol. Syst. 18: 269–292.Google Scholar
  37. Neff, N. A. (1982).The Big Cats: The Paintings of Guy Coheleach. Abrams, New York.Google Scholar
  38. Nei, M., and Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases.Proc. Natl. Acad. Sci. USA 76: 5269–5273.PubMedGoogle Scholar
  39. Nei, M., and Tajima, F. (1985). Evolutionary change of restriction cleavage sites and phylogenetic inference for man and apes.Mol. Biol. Evol. 2: 189–205.PubMedGoogle Scholar
  40. O'Brien, S. J. (1986). Molecular genetics in the domestic cat and its relatives.Trends Genet. 2: 137–142.Google Scholar
  41. O'Brien, S. J. (1994a). Genetic and phylogenetic analyses of endangered species.Annu. Rev. Genet. 28: 467–489.PubMedGoogle Scholar
  42. O'Brien, S. J. (1994b). A role for molecular genetics in biological conservation.Proc. Natl. Acad. Sci. USA 91: 5748–5755.PubMedGoogle Scholar
  43. O'Brien, S. J., Collier, G. E., Benveniste, R. E., Nash, W. G., Newman, A. K., Simonson, J. M., Eichelberger, M. A., Seal, U. S., Bush, M., and Wildt, D. E. (1987). Setting the molecular clock in Felidae: The great cats,Panthera. In:Tigers of the World, R. L. Tilson, ed., pp. 10–27, Noyes, Park Ridge, NJ.Google Scholar
  44. O'Brien, S. J., Roelke, M. E., Yuhki, N., Richards, K. W., Johnson, W. E., Franklin, W. L., Anderson, A. E., Bass, O. L., Jr., Belden, R. C., and Martenson, J. S. (1990). Genetic introgression within the Florida pantherFelis concolor coryi.Natl. Geogr. Res. 6: 485–494.Google Scholar
  45. O'Brien, S. J., Martenson, J. S., Johnson, W. E., Miththapala, S., Janczewski, D. N., Pecon Slattery, J., Gilbert, D. A., Packer, C., Roelke, M. E., Bush, M., and Wildt, D. E. (1996). Conservation genetics of the Felidae: In:Conservation Genetics of Rare and Endangered Species, J. C. Avise and J. Hamrick, eds., pp. 50–74, Chapman and Hall, NY.Google Scholar
  46. Pecon Slattery, J., Johnson, W. E., Goldman, D., O'Brien, S. J. (1994). Phylogenetic reconstruction of South American felids defined by protein electrophoresis.J. Mol. Evol. 39: 296–305.PubMedGoogle Scholar
  47. Randi, E., and Ragni, B. (1991). Genetic variability and biochemical systematics of domestic and wild cat populations (Felis silvestris: Felidae).J. Mammal. 72: 79–88.Google Scholar
  48. Reeves, R. H., and O'Brien, S. J. (1984). Molecular genetic characterization of the RD-114 gene family of endogenous feline retroviral sequences.J. Virol. 52: 164–171.PubMedGoogle Scholar
  49. Salles, L. O. (1992). Felid phylogenetics: Extant taxa and skull morphology (Felidae, Aeluroidea).Am. Mus. Novit. 3047: 1–67.Google Scholar
  50. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989).Molecular Cloning, a Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  51. Savage, D. E., and Russell, D. E. (1983).Mammalian Paleofaunas of the World, Addison-Wesley, London.Google Scholar
  52. Seidensticker, J., and Lumpkin, S. (eds.) (1991).Great Cats: Majestic Creatures of the Wild, Weldon Owen, Sydney, Australia.Google Scholar
  53. Swofford, D. L. (1993).PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1.1. Computer program, Smithsonian Institute, Washington, DC.Google Scholar
  54. Templeton, A. R. (1983). Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes.Evolution 37: 221–244.Google Scholar
  55. Turner, A. (1987). New fossil carnivore remains from the Sterkfontein hominid site (Mammalia: Carnivora).Ann: Transvaal. Mus. 34: 319–347.Google Scholar
  56. Wayne, R. K., Benveniste, R. E., Janczewski, D. N., and O'Brien, S. J. (1989). Molecular and biochemical evolution of the Carnivora. In:Carnivore Behavior, Ecology and Evolution, J. L. Gittleman, ed., pp. 465–494. Cornell University Press, Ithaca, NY.Google Scholar
  57. Wayne, R. K., Van Valkenburgh, B., and O'rrien, S. J. (1991). Molecular distance and divergence time in carnivores and primates.Mol. Biol. Evol. 8: 297–319.PubMedGoogle Scholar
  58. Werderlin, L. (1985). Small Pleistocene felines of North America.J. Vert. Paleo. 5: 194–210.Google Scholar
  59. Wilson, A. C., Cann, R. L., Carr, S. M., George, M., Gyllensten, U. B., Helm-Bychowski, K. M., Higuchi, R. G., Palumbi, S. R., Prager, E. M., Sage, R. D., and Stoneking, M. (1985). Mitochondrial DNA and two perspectives on evolutionary genetics.Biol. J. Linn. Soc. 26: 375–400.Google Scholar
  60. Wolpoff, M. (1989). Multiregional evolution: The fossil alternative to Eden. In:The Human Revolution: Behavioural and Biological Perspectives on the Origins of Modern Humans, P. Mellars and C. Stringer eds., pp. 62–108, Princeton University Press, Princeton, NJ.Google Scholar
  61. Wozencraft, M. (1993). Order Carnivora: In:Mammal Species of the World, 2nd ed., D. E. Wilson, and D. M. Reeder, eds., pp. 279–348, Smithsonian Institution Press, Washington, DC.Google Scholar
  62. Wu, C.-I. (1991): Inferences of species phylogeny in relation to segregation of ancient polymorphisms.Genetics 127: 429–435.PubMedGoogle Scholar
  63. Wurster-Hill, D. H., and Centerwall, W. R. (1982). The interrelationships of chromosome banding patterns in canids, mustelids, hyena, and felids.Cytogenet. Cell Genet. 15: 306–331.Google Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • Warren E. Johnson
    • 1
  • Peter A. Dratch
    • 2
  • Janice S. Martenson
    • 1
  • Stephen J. O'Brien
    • 1
  1. 1.Laboratory of Viral CarcinogenesisNCI-Frederick Cancer Research and Development CenterFrederick
  2. 2.Biological Carcinogenesis and Development ProgramSAIC NCI-Frederick Cancer Research and Development CenterFrederick
  3. 3.National Fish and Wildlife Forensic LaboratoryAshland

Personalised recommendations