Skip to main content

Phylogenetic reconstruction of the felidae using 16S rRNA and NADH-5 mitochondrial genes

Abstract

The Felidae family represents a challenge for molecular phylogenetic reconstruction because it consists of 38 living species that evolved from a relatively recent common ancestor (10–15 million years ago). We have determined mitochondrial DNA sequences from two genes that evolve at relatively rapid evolutionary rates, 16S rRNA (379 bp) and NADH dehydrogenase subunit 5 (NADH-5, 318 bp), from multiple individuals of 35 species. Based on separate and combined gene analyses using minimum evolution, maximum parsimony, and maximum likelihood phylogenetic methods, we recognized eight significant clusters or species clades that likely reflect separate monophyletic evolutionary radiations in the history of this family. The clusters include (1) ocelot lineage, (2) domestic cat lineage, (3) Panthera genus, (4) puma group, (5) Lynx genus, (6) Asian leopard cat group, (7) caracal group, and (8) bay cat group. The results confirm and extend previously hypothesized associations in most cases, but in others, e.g., the bay cat group, suggest novel phylogenetic relationships. The results are compared and evaluated with molecular, cytogenetic, and morphological data to derive a phylogenetic synthesis of field evolutionary history.

This is a preview of subscription content, access via your institution.

References

  1. Adams DB (1979) The cheetah: native American. Science 205:1155–1158

    PubMed  Article  Google Scholar 

  2. Avise JC (1994) Molecular markers, natural history and evolution. Chapman and Hall, New York

    Google Scholar 

  3. Benveniste RE, Todaro GJ (1974) Homology between type-C viruses of various species as determined by molecular hybridization. Proc Natl Acad Sci USA 70:3316–3320

    Article  Google Scholar 

  4. Benveniste RE, Sherr CJ, Todaro GJ (1975) Evolution of type C viral genes: origin of feline leukemia virus. Science 190:886–888

    PubMed  Article  CAS  Google Scholar 

  5. Benveniste RE (1985) The contributions of retroviruses to the study of mammalian evolution. In: Maclntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 359–417

    Google Scholar 

  6. Berta A (1983) A new species of small cat (Felidae) from the late Pliocene-early Pleistocene Uquian of Argentinian. J Mammal 64: 720–725

    Article  Google Scholar 

  7. Clutton-Brock J (1987) A natural history of domesticated animals. Cambridge University Press, Cambridge, England

    Google Scholar 

  8. Collier GE, O’Brien SJ (1985) A molecular phylogeny of the Felidae: immunological distance. Evolution 39:437–487

    Article  Google Scholar 

  9. Engelke DR, Hoener PA, Collins FS (1988) Direct sequencing of enzymatically amplified human genomic DNA. Proc Natl Acad Sci USA 85:544–548

    PubMed  Article  CAS  Google Scholar 

  10. Ewer RF (ed) (1973) The carnivores. Cornell University Press, Ithaca, NY 409 pp.

    Google Scholar 

  11. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    PubMed  Article  CAS  Google Scholar 

  12. Felsenstein J (1993) Phylogeny inference package (PHYLIP). Version 3.5. University of Washington, Seattle

    Google Scholar 

  13. Ficcarelli G (1984). The Villafranchian cheetahs from Tuscany and remarks on the dispersal and evolution of the genus Acinonyx. Palaeontographia Italica 73:94–103

    Google Scholar 

  14. Glass GE, Martin LD (1978) A multivariate comparison of some extant and fossil Felidae, Carnivora. Carnivora 1:80–88

    Google Scholar 

  15. Hemmer H (1978) The evolutionary systematics of living Felidae: present status and current problems. Carnivore 1:71–79

    Google Scholar 

  16. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Google Scholar 

  17. Hillis DM (1995) Approaches for assessing phylogenetic accuracy. Syst Biol 44:3–16

    Google Scholar 

  18. Hoelzel AR, Green A (1992) Analysis of population-level variation by sequencing PCR-amplified DNA. In: Hoelzel AR (ed) Molecular genetic analysis of populations, a practical approach. IRL Press, Oxford pp. 159–187

    Google Scholar 

  19. Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Syst Biol 42:247–264

    Google Scholar 

  20. Huelsenbeck JP, Bull JJ, Cunningham CW (1996) Combining data in phylogenetic analysis. Trends Ecol Evol 11:152–157

    Article  Google Scholar 

  21. Hunt MH (1996) Biogeography of the order Carnivora. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution, vol 2. Cornell University Press, Ithaca, NY, pp. 485–541

    Google Scholar 

  22. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    PubMed  CAS  Google Scholar 

  23. Janczewski DN, Modi WS, Stephens JC, O’Brien SJ (1995) Molecular evolution of mitochondrial 12S RNA and cytochrome b sequences in the Pantherine lineage of Felidae. Mol Biol Evol 12:690–707

    PubMed  CAS  Google Scholar 

  24. Johnson WE, Dratch PA, Martenson JS, O’Brien SJ (1996) Resolution of recent radiations within three evolutionary lineages of Felidae using mitochondrial restriction fragment length polymorphism variation. J Mammal Evol 3:97–120

    Article  Google Scholar 

  25. Johnson WE, Culver M, Warte A, O’Brien SJ (submitted) Tracking the evolution of the elusive Andean Mountain Cat (Oreailurus jacobita) from mitochondrial DNA. J Heredity

  26. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    PubMed  Article  CAS  Google Scholar 

  27. Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis of relationships among Epiarates (Boidae, Serpentes) Syst Zool 38:7–25

    Google Scholar 

  28. Kumar S, Tamura K, Nei M (1993) MEGA: Molecular evolutionary genetics analysis, version 1.01. The Pennsylvania State University, University Park, PA

    Google Scholar 

  29. Kurten B (1968) Pleistocene mammals of Europe. Aldine Press, Chicago

    Google Scholar 

  30. Kurten B, Anderson E (1980) In: Pleistocene mammals of North America. Columbia University Press, New York, pp. 108–118

    Google Scholar 

  31. Leyhausen P (1979) Cat behavior. Garland Press, New York

    Google Scholar 

  32. Lopez JV, Yuhki N, Masuda R, Modi W, O’Brien SJ (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

    PubMed  CAS  Google Scholar 

  33. Lopez JV, Cevario S, O’Brien SJ (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

    PubMed  Article  CAS  Google Scholar 

  34. Lopez JV, Culver M, Stephens JC, Johnson WE, O’Brien SJ (submitted) Rates of nuclear and cytoplasmic mitochondrial DNA sequence divergence in mammals. Mol Biol Evol

  35. MacFadden BJ, Galiano H (1981) Late Hemphillian cat (Mammalia: Felidae) from the Bone Valley Formation of central Florida. J Paleontolo 55:218–226

    Google Scholar 

  36. Martin LD (1980) Functional morphology and the evolution of cats. Trans Neb Acad Sci 13:141–154

    Google Scholar 

  37. Martin LD (1989) Fossil history of the terrestrial Carnivora. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Cornell University Press, Cornell, NY, pp 536–568

    Google Scholar 

  38. Masuda RM, Lopez JV, O’Brien SJ, Pecon Slattery J, Yuhki N, O’Brien SJ (in press) Molecular phylogeny of mitochondrial cytochrome b and 12S rRNA sequences in the Felidae: ocelot and domestic cat lineages. Mol Phyl Evol

  39. Modi WS, Nash WG, Ferrari AC, O’Brien SJ (1987) Cytogenetic methodologies for gene mapping and comparative analyses in mammalian cell culture systems. Gene Anal Tech 4:75–85

    PubMed  Article  CAS  Google Scholar 

  40. Modi WS, O’Brien SJ (1988) Quantitative cladistic analysis of chromosomal banding among species in three orders of mammals: hominoid primates, felids and arvicolid rodents. In: Gustafson JP, Appels R (eds) Chromosome structure and function. Plenum Press, New York

    Google Scholar 

  41. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    PubMed  Article  CAS  Google Scholar 

  42. Neff NA (1982) The big cats: the paintings of Guy Coheleach. Abrams Press, New York

    Google Scholar 

  43. Neigel JE, Avise JC (1986) Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. In: Karlin S, Nevo E (eds) Evolutionary processes and theory. Academic Press, Orlando, FL

    Google Scholar 

  44. Nowak RM (1991) Walker’s mammals of the world, vol 2. John Hopkins University Press, Baltimore

    Google Scholar 

  45. O’Brien SJ, Collier GE, Benveniste RE, Nash WG, Newman AK, Simonson JM, Eichelberger MA, Seal US, Janssen D, Bush M, Wildt DE (1987) Setting the molecular clock in Felidae: the great cats, Panthern. In: Tilson RL, Seal US (eds) Tigers of the world. Noyes, NJ, pp 10–27

    Google Scholar 

  46. Orr PC (1969) Felis trumani, a new radiocarbon dated cat skull from Crypt Cave, Nevada. Santa Barbara Mus Nat Hist Bull 2:1–8

    Google Scholar 

  47. Patterson B, Pascual R (1972) The fossil mammal fauna of South American. In: Keast A, Erk C, Glass B (eds) Evolution, mammals and southern continents. State University of New York Press, Albany, NY, pp 247–309

    Google Scholar 

  48. Pecon Slattery J, Johnson WE, Goldman D, O’Brien SJ (1994) Phylogenetic reconstruction of South American felids defined by protein electrophoresis. J Mol Evol 39:296–305

    Article  Google Scholar 

  49. Peters G, Hast MH (1994) Hyoid structure, laryngeal anatomy, and vocalization in fields (Mammalia: Carnivora: Felidae). Z Saugetierkunde 59:87–104

    Google Scholar 

  50. Pocock, RI (1932) The marbled cat (Pardofelis marmorata) and some other Oriental species, with the definition of a new genus of the Felidae. Proc Zool Soc London 132:741–766

    Google Scholar 

  51. Randi E, Ragni B (1991) Genetic variability and biochemical systematics of domestic and wild cat populations (Felis silvestris: Felidae). J Mamm 72:79–88

    Article  Google Scholar 

  52. Reeves RH, O’Brien SJ (1984) Molecular genetic characterization of the RD-114 gene family of endogenous feline retroviral sequences of the domestic cat. J Virol 52:164–171

    PubMed  CAS  Google Scholar 

  53. Saiki RK, Scharf S, Fallona F, Mullis KB, Horn GT, Erlich HA, Arnheim N (1985) Enzymatic amplification of B-globin genomic sequences and restriction site analysis for diagnosis of sickle-cell anemia. Science 230:1350–1354

    PubMed  Article  CAS  Google Scholar 

  54. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–426

    PubMed  CAS  Google Scholar 

  55. Salles LO (1992) Felid phylogenetics: extant taxa and skull morphology (Felidae, Aeluroidae). Am Mus Novit 3047:1–67

    Google Scholar 

  56. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a lab manual. 2nd ed. Cold Spring Harbor Laboratory publications, Cold Spring Harbor, NY

    Google Scholar 

  57. Savage DE, Russell DE (1983) Mammalian paleofaunas of the world. Addison-Wesley, London

    Google Scholar 

  58. Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisae, Schizosaccharomyces pombe, Drosophila melanogaster, and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res 16:8207–8211

    PubMed  Article  CAS  Google Scholar 

  59. Sibley SG, Ahlquist JE (1987) DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. J Mol Evol 26:99–121

    PubMed  Article  CAS  Google Scholar 

  60. Sourdis J, Nei M (1988) Relative efficiencies of the maximum parsimony and distance-matrix methods in obtaining the correct tree. Mol Biol Evol 5:298–311

    PubMed  CAS  Google Scholar 

  61. Swofford DL (1993) Phylogenetic analysis using parsimony (PAUP), version 3.1.1. University of Illinois, Champaign

    Google Scholar 

  62. Turner A (1985) Extinction, speciation and dispersal in African larger carnivores from the late Miocene to Recent. S Afr J Sci 81:256–257

    Google Scholar 

  63. Turner A (1987) New fossil carnivore remains from the Sterkfontein hominid site (Mammalia: Camivora). Ann Transvall Mus 34:319–347

    Google Scholar 

  64. Umbgrove JHF (1949) Structural history of the East Indies. Cambridge University Press, Cambridge, England

    Google Scholar 

  65. Van Valkenburgh B, Grady F, Kurten B (1990) The Plio-Pleistocene cheetah-like cat Miracinonyx inexpectatus of North America. J Vert Paleo 10:434–454

    Google Scholar 

  66. Werdelin L (1985) Small pleistocene felines of North America. J Vert Paleo 5:194–210

    Google Scholar 

  67. Wozencraft C (1993) Order Carnivora, Family Felidae. In: Wilson DE, Reeder DA (eds) Mammal species of the world. Smithonsian Institution Press, 2nd edition. Washington, DC, pp 288–299

    Google Scholar 

  68. Wu CI (1991) Inference of species phylogeny in relation to segregation of ancient polymorphisms. Genetics 127:429–435

    PubMed  CAS  Google Scholar 

  69. Wurster-Hill DH, Centerwall WR (1982) The interrelationships of chromosome banding patterns in Procyonids, Viverrids and Felids. Cytogenet Cell Genet 34:178–192

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Warren E. Johnson or Stephen J. O’Brien.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Johnson, W.E., O’Brien, S.J. Phylogenetic reconstruction of the felidae using 16S rRNA and NADH-5 mitochondrial genes. J Mol Evol 44, S98–S116 (1997). https://doi.org/10.1007/PL00000060

Download citation

Key words

  • Phylogeny
  • 16S rRNA
  • NADH dehydrogenase subunit 5 (NADH-5)
  • Mitochondrial sequence data
  • Felidae