Skip to main content
SpringerLink
Log in

Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: Convincing evidence for several superordinal clades

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Phylogenetic relationships of 25 mammalian species representing 17 of the 18 eutherian orders were examined using DNA sequences from a 1.2-kb region of the 5′ end of exon 1 of the single-copy nuclear gene known as interphotoreceptor retinoid binding protein (IRBP). A wide variety of methods of analysis of the DNA sequence, and of the translated products, all supported a five-order clade consisting of elephant shrew (Macroscelidea)/aardvark (Tubulidentata)/and the paenungulates (hyracoids, sirenians, and elephants), with bootstrap support in all cases of 100%. The Paenungulata was also strongly supported by these IRBP data. In the majority of analyses this monophyletic five-order grouping was the first branch off the tree after the Edentata. These results are highly congruent with two other recent sources of molecular data. Another superordinal grouping, with similar 100% bootstrap support in all of the same wide-ranging types of analyses, was Artiodactyla/Cetacea. Other superordinal affinities, suggested by the analyses, but with less convincing support, included a Perissodactyla/Artiodactyla/Cetacea clade, an Insectivora/Chiroptera clade, and Glires (an association of rodents and lagomorphs).

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

References

  • Adachi J, Cao Y, Hasegawa M (1993) Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: rapid evolution in warm blooded vertebrates. J Mal Evol 36:270–281

    CAS  Google Scholar 

  • Adkins RM, Honeycutt RL (1991) Molecular phylogeny of the superorder Archonta. Proc Natl Acad Sci USA 88:10317–10321

    CAS  PubMed  Google Scholar 

  • Adkins RM, Honeycutt RL (1993) A molecular examination of Archontan and Chiropteran monophyly. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum, New York, pp 227–249

    Google Scholar 

  • Allard MW, McNiff BE, Miyamoto MM (1996) Support for interordinal eutherian relationships with an emphasis on Primates and their archontan relatives. Mol Phyl Evol 5:78–88

    CAS  Google Scholar 

  • Ammerman LK, Hillis DM (1992) A molecular test of bat relationships: monophyly or diphyly? Syst Biol 41:222–232

    Google Scholar 

  • Bailey WJ, Slightom JL, Goodman M (1992) Rejection of the “flying primate” hypothesis by phylogenetic evidence from the ε-globin gene. Science 256:86–89

    CAS  PubMed  Google Scholar 

  • Borst DE, Redmond TM, Elser JE, Gonda MA, Wiggert B, Chader GJ, Nickerson JM (1989) Interphotoreceptor retinoid binding protein: gene characterization, protein repeat structure, and its evolution. J Biol Chem 264:1115–1123

    CAS  PubMed  Google Scholar 

  • Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci 5:233–234

    CAS  PubMed  Google Scholar 

  • Cao Y, Adachi J, Janke A, Pääbo S, Hasegawa M (1994) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39:519–527

    Article  CAS  PubMed  Google Scholar 

  • Corbet GB, Hanks J (1968) A revision of the elephant shrews, family Macroscelididae. Bull Br Mus Nat Hist Zool 16:47–111

    Google Scholar 

  • Czelusniak J, Goodman M, Koop BF, Tagle DA, Shoshani J, Braunitzer G, Kleinschmidt TK, de Jong WW, Matsuda G (1990) Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of Eutheria. In: Genoways HH (ed) Current mammalogy, vol 2. Plenum, New York, pp 545–572

    Google Scholar 

  • de Jong WW, Leunissen JAM, Wistow GJ (1993) Eye lens crystalline and the phylogeny of placental orders: evidence for a Macroscelid-Paenungulate Glade? In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny: placentals. Springer Verlag, New York, pp 5–12

    Google Scholar 

  • de Jong WW, Zweers A, Goodman M (1981) Relationship of aardvark to elephants, hyraxes and sea cows from alpha-crystallin sequences. Nature 292:538–540

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985a) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1985b) Confidence limits on phylogenies with a molecular clock. Syst Zool 34:152–161

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (phylogeny inference package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Fong S-L, Fong W-B, Moms TA, Kedzie KM, Bridges CDB (1990) Characterization and comparative structural features of the gene for human interstitial retinol-binding protein. J Biol Chem 265:3648–3653

    CAS  PubMed  Google Scholar 

  • Gingerich PD, Smith BH, Simons EL (1990) Hind limbs of EoceneBasilosaurus: evidence of feet in whales. Science 249:154–157

    Google Scholar 

  • Goodman M, Czelusniak J, Beeber JE (1985) Phylogeny of primates and other eutherian orders: a cladistic analysis using amino acid and nucleotide sequence data. Cladistics 1:171–185

    Google Scholar 

  • Graur D, Higgins DG (1994) Molecular evidence for the inclusion of cetaceans within the order Artiodactyla. Mol Biol Evol 11:357–364

    CAS  PubMed  Google Scholar 

  • Gregory WK (1910) The orders of mammals. Bull Am Mus Nat Hist 27:1–524

    Google Scholar 

  • Hartenberger JL (1986) Hypothèse paléontologique sur l'orìgine des Macroscelidea (Manmialia). C R Acad Sci Ser II 302:247–249

    Google Scholar 

  • Honeycutt RL, Adkins RM (1993) Higher level systematics of eutherian mammals: An assessment of molecular characters and phylogenetic hypotheses. Annu Rev Ecol Syst 24:279–305

    Article  Google Scholar 

  • Honeycutt RL, Nedbal MA, Adkins RM, Janacek LL (1995) Mammalian mitochondrial DNA evolution: a comparison of the cytochromeb and cytochromec oxidase II genes. J Mol Evol 40:260–272

    Article  CAS  PubMed  Google Scholar 

  • Johnson JI, Kirsch JAW (1993) Phylogeny through brain traits: interordinal relationships among mammals including Primates and Chiroptera. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum, New York, pp 293–331

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 2. Academic Press, New York, pp 21–123

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li W-H, Gouy M, Sharp PM, O'Huigin C, Yang Y-W (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla and Carnivora and molecular clocks. Proc Natl Acad Sci USA 87:6703–6707

    CAS  PubMed  Google Scholar 

  • McKenna MC (1975) Toward a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates, a multidisciplinary approach. Plenum, New York, pp 21–46

    Google Scholar 

  • McKenna MC (1987) Molecular and morphological analysis of highlevel mammalian interrelationships. In: Patterson C (ed) Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, Cambridge, pp 55–93

    Google Scholar 

  • Milinkovitch MC, Orti G, Meyer A (1993) Revised phylogeny of whales suggested by mitochondrial ribosomal DNA sequences. Nature 361:346–348

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto MM, Goodman M (1986) Biomolecular systematics of eutherian mammals: phylogenetic patterns and classification. Syst Zool 35:230–240

    Google Scholar 

  • Nei M (1991) Relative efficiencies of different tree-making methods for molecular data. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, Oxford, pp 90–128

    Google Scholar 

  • Novacek MJ (1982) Information for molecular studies from anatomical and fossil evidence on eutherian phylogeny. In: Goodman M (ed) Macromolecular sequences in systematic and evolutionary biology. Plenum, New York, pp 3–41

    Google Scholar 

  • Novacek MJ (1986) The skull of leptictid insectivorans and the higherlevel classification of eutherian mammals. Bull Am Mus Nat Hist 183:1–111

    Google Scholar 

  • Novacek MJ (1990) Morphology, paleontology, and the higher Glades of mammals. In: Genoways HH (ed) Current mammalogy, vol 2. Plenum, New York, pp 507–543

    Google Scholar 

  • Novacek MJ (1992) Mammalian phylogeny: shaking the tree. Nature 356:121–125

    Article  CAS  PubMed  Google Scholar 

  • Novacek MJ, Wyss AR (1986) Higher level relationships of the recent eutherian orders: morphological evidence. Cladistics 2:257–287

    Google Scholar 

  • Pepperberg DR, Okajima T-IL, Wiggert B, Ripps H, Crouch RK, Chader GJ (1993) Interphotoreceptor retinoid binding protein (IRBP): molecular biology and physiological role in the visual cycle of rhodopsin. Mol Neurobiol 7:61–84

    CAS  PubMed  Google Scholar 

  • Porter CA, Goodman M, Stanhope MJ (1996) Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand factor gene. Mol Phylo Evol 5:89–101

    CAS  Google Scholar 

  • Prothero DR, Manning EM, Fischer M (1988) The phylogeny of ungulates. In: Benton MJ (ed) The phylogeny and classification of the tetrapods, vol 2. Clarendon, Oxford, pp 201–234

    Google Scholar 

  • Prothero DR, Schoch R (1989) Origin and evolution of the Perissodactyla: summary and synthesis. In: Prothero DR, Schoch R (eds) The evolution of the Perissodactyls. Oxford University Press, New York, pp 504–529

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Shoshani J (1993) Hyracoidea-Tethytheria affinity based on myological data. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny: placentals. Springer Verlag, New York, pp 235–256

    Google Scholar 

  • Simons EL, Holroyd PA, Bown TM (1991) Early tertiary elephant shrews from Egypt and the origin of the Macroscelidea. Proc Natl Acad Sci USA 88:9734–9737

    CAS  PubMed  Google Scholar 

  • Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 851–350

    Google Scholar 

  • Springer MS, Kirsch JAW (1993) A molecular perspective on the phylogeny of placental mammals based on mitochondrial 12S rDNA sequences, with special reference to the problem of the Paenungulata. J Mammal Evol 1:149–166

    Article  Google Scholar 

  • Stanhope MJ, Czelusniak J, Si J-S, Nickerson J, Goodman M (1992) A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. Mol Phyl Evol 1:148–160

    CAS  Google Scholar 

  • Stanhope MJ, Bailey WJ, Czelusniak J, Goodman M, Si J-S, Nickerson J, Sgouros JG, Singer GAM, Kleinschmidt K (1993) A molecular view of primate supraordinal relationships from the analysis of both nucleotide and amino acid sequences. In: MacPhee RDE (ed) Primates and their relatives in phylogenetic perspective. Plenum, New York, pp 251–292

    Google Scholar 

  • Szalay FS (1977) Phylogenetic relationships and classification of the eutherian Mammalia. In: Hecht MK, Goody PC, Hecht BM (eds) Major patterns in vertebrate evolution. Plenum, New York, pp 315–374

    Google Scholar 

  • Szalay FS (1985) Rodent and lagomorph morphotype adaptations, origins, and relationships: some postcranial attributes analyzed. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents: a multidisciplinary analysis. Plenum, New York, pp 83–132

    Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biology and Biochemistry, Queen's University, 97 Lisburn Rd., BT9 07BL, Belfast, UK

    Michael J. Stanhope & Victor G. Waddell

  2. Oceanographic Center, Nova Southeastern University, 33004, Dania, 8000 N Ocean Dr., FL, USA

    Marta R. Smith & Mahmood S. Shivji

  3. Department of Anatomy, Wayne State University, 550 East Canfield Ave., 48201, Detroit, MI, USA

    Calvin A. Porter & Morris Goodman

Authors
  1. Michael J. Stanhope
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta R. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor G. Waddell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Calvin A. Porter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mahmood S. Shivji
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Morris Goodman
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: M. J. Stanhope

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stanhope, M.J., Smith, M.R., Waddell, V.G. et al. Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: Convincing evidence for several superordinal clades. J Mol Evol 43, 83–92 (1996). https://doi.org/10.1007/BF02337352

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02337352

Key words

Search

Navigation