Abstract
Phylogenetic relationships among various primate groups were examined based on sequences of ε-globin genes. ε-globin genes were sequenced from five species of strepsirhine primates. These sequences were aligned and compared with other known primate ε-globin sequences, including data from two additional strepsirhine species, one species of tarsier, 19 species of New World monkeys (representing all extant genera), and five species of catarrhines. In addition, a 2-kb segment upstream of the ε-globin gene was sequenced in two of the five strepsirhines examined. This upstream sequence was aligned with five other species of primates for which data are available in this segment. Domestic rabbit and goat were used as outgroups. This analysis supports the monophyly of order Primates but does not support the traditional prosimian grouping of tarsiers, lorisoids, and lemuroids; rather it supports the sister grouping of tarsiers and anthropoids into Haplorhini and the sister grouping of lorisoids and lemuroids into Strepsirhini. The mouse lemur (Microcebus murinus) and dwarf lemur (Cheirogaleus medius) appear to be most closely related to each other, forming a clade with the lemuroids, and are probably not closely related to the lorisoids, as suggested by some morphological studies. Analysis of the ε-globin data supports the hypothesis that the aye-aye (Daubentonia madagascariensis) shares a sister-group relationship with other Malagasy strepsirhines (all being classified as lemuroids). Relationships among ceboids agree with findings from a previous ε-globin study in which fewer outgroup taxa were employed. Rates of molecular evolution were higher in lorisoids than in lemuroids.
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References
Adkins RM, Honeycutt RL (1994) Evolution of the primate cytochrome c oxidase subunit II gene. J Mol Evol 38:215–231
Bailey WJ, Fitch DA, Tagle DA, Czelusniak J, Slightom JL, Goodman M (1991) Molecular evolution of the ψη-globin gene locus: Gibbon phylogeny and the hominoid slowdown. Mol Biol Evol 8:155–184
Bailey WJ, Slightom JL, Goodman M (1992a) Rejection of the “flying primate” hypothesis by phylogenetic evidence form the ε-globin gene. Science 256:86–89
Bailey WJ, Hayasaka K, Skinner C, Kehoe S, Sieu L, Slightom JL, Goodman M (1992b) Reexamination of the African hominoid trichotomy with additional sequences from the primate β-globin gene cluster. Mol Phyl Evol 1:97–135 Bonner TI, Heinemann R, Todaro GJ (1980) Evolution of DNA sequences has been retarded in Malagasy primates. Nature 286:420423
Bonner TI, Heinemann R, Todaro GJ (1981) A geographical factor involved in the evolution of the single copy DNA, sequence of primates. In: Scudder GGE, Reveal JL (eds) Evolution today. Hunt Institute for Botanical Documentation, Pittsburgh, pp 293–300
Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393–1398
Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput Appl Biosci 5:233–234
Charles-Dominique P, Martin RD (1970) Evolution of lorises and lemurs. Nature 227:257–260
Collins FS, Weissman SM (1984) The molecular genetics of human hemoglobin. Prog Nucleic Acid Res Mol Biol 31:315–462
Corbet GB, Hill JE (1991) A world list of mammalian species, 3rd edition. Nat. Hist. Mus. Publ., Oxford Univ. Press, Oxford
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 Press, New York, pp 545–572
Dene H, Goodman M, Prychodko W (1976) Immunodiffusion evidence on the phylogeny of the primates. In: Goodman M, Tashian RE (eds) Molecular anthropology. Plenum, New York, pp 171–195
Dene H, Goodman M, Prychodko W (1980) Immunodiffusion systematics of the Primates. IV. Lemuriformes. Mammalia 44:211–223
Fleagle JG (1988) Primate adaptation & evolution. Academic Press, San Diego, California
Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Mol Biol 38:105–164
Goodman M (1985) Rates of molecular evolution: the hominoid slowdown. Bioessays 3:9–14
Goodman M, Czelusniak J, Moore GW, Romero-Herrara AJ, Matsuda G (1979) Fitting the gene lineage into its species lineages: a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool 28:132–163
Goodman M, Koop BF, Czelusniak J, Weiss ML, Slightom JL (1984) The η-globin gene: its long evolutionary history in the β-globin gene family of mammals. J Mol Biol 180:803–823
Goodman M, Bailey WJ, Hayasaka K, Stanhope MJ, Slightom J, Czelusniak J (1994) Molecular evidence on primate phylogeny from DNA sequences. Am J Phys Anthropol 94:3–24
Groves CP (1974) Taxonomy and phylogeny of prosimians. In: Martin RD, Doyle GA, Walker AC (eds) Prosimian biology. Duckworth, London, pp 435–448
Groves CP (1989) A theory of human and primate evolution. Clarendon Press, Oxford
Hardison RC (1983) The nucleotide sequence of the rabbit embryonic globin gene β4. J Biol Chem 258:8739–8744
Harris S, Thackeray JR, Jeffreys AJ, Weiss ML (1986) Nucleotide sequence analysis of the lemur β-globin gene family: evidence for major rate fluctuations in globin polypeptide evolution. Mol Biol Evol 3:465–484
Higgins DG, Bleasby AJ, Fuchs R (1992) Clustal V: improved software for multiple sequence alignment. CABIOS 8:189–191
Honacki JH, Kinman KE, Koeppl JW (1982) Mammal species of the world: a taxonomic and geographic reference. Allen Press, Lawrence, Kansas
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
Koop BF, Miyamoto MM, Embury JE, Goodman M, Czelusniak J, Slightom JL (1986) Nucleotide sequence and evolution of the orangutan globin gene region and surrounding Alu repeats. J Mol Evol 24:94–102
Koop BF, Tagle DA, Goodman M, Slightom JL (1989) A molecular view of primate phylogeny and important systematic and evolutionary questions. Mol Biol Evol 6:580–612
Longmire JL, Lewis AK, Brown NC, Buckingham JM, Clark LM, Jones MD, Meincke LJ, Meyne J, Ratliff RL, Ray FA, Wagner RP, Moyzis RK (1988) Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics 2:14–24
Martin RD (1990) Primate origins and evolution. Chapman and Hall, London
Moore GW, Barnabas J, Goodman M (1973) A method for constructing maximum parsimony ancestral amino acid sequences on a given network. J Theor Biol 38:459–485
Nowak RM (1991) Walker's mammals of the world, fifth edition. Johns Hopkins University Press, Baltimore
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Schneider H, Schneider MPC, Sampaio I, Harada ML, Stanhope M, Czelusniak J, Goodman M (1993) Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol Phyl Evol 2:225–242
Schwartz JH, Tattersall I (1985) Evolutionary relationships of living lemurs and lorises (Mammalia, Primates) and their potential affinities with European Eocene Adapidae. Anthropol Pap Am Mus Nat Hist 57:344–352
Shapiro SG, Schon EA, Townes TM, Lingrel JB (1983) Sequence and linkage of the goat εII and εII β-globin genes. J Mol Biol 169:31–52
Simpson GG (1945) The principles of classification and a classification of the mammals. Bull Am Mus Nat Hist 85:1–350
Szalay FS, Katz CC (1973) Phylogeny of lemurs, galagos and lorises. Folia Primatol 19:88–103
Tagle DA, Koop BF, Goodman M, Slightom JL, Hess DL, Jones RT (1988) Embryonic ε and γ globin genes of a prosimian primate (Galago crassicaudatus), nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J Mol Biol 203:439–445
Wilson DE, Reeder DM (1993) Mammal species of the world: a taxonomic and geographic reference. Smithsonian Institution Press, Washington
Yoder AD (1994) Relative position of the Cheirogaleidae in Strepsirhine phylogeny: a comparison of morphological and molecular methods and results. Am J Phys Anthropol 94:25–46
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Correspondence to: M. Goodman
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Porter, C.A., Sampaio, I., Schneider, H. et al. Evidence on primate phylogeny from ε-globin gene sequences and flanking regions. J Mol Evol 40, 30–55 (1995). https://doi.org/10.1007/BF00166594
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DOI: https://doi.org/10.1007/BF00166594