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Molecular Systematics of Higher Primates: Genealogical Relations

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Molecular Systematics of Higher Primates: Genealogical Relations Proc. Nati. Acad. Sci. USA Vol. 85, pp. 7627-7631, October 1988 Evolution Molecular systematics of higher primates: Genealogical relations and classification (DNA sequences/rhesus macaque/human evolution/phylogeny/globin gene region) MICHAEL M. MIYAMOTO*t, BEN F. Koopf, JERRY L. SLIGHTOM§1, MORRIS GOODMAN¶, AND MICHELE R. TENNANT11 *Department of Zoology, University of Florida, Gainesville, FL 32611; Departments of tMolecular Biology and Genetics and lAnatomy and Cell Biology, Wayne State University School of Medicine, Detroit, MI 48201; §Division of Molecular Biology, The Upjohn Company, Kalamazoo, MI 49001; and I'Department of Biological Sciences, Wayne State University, Detroit, MI 48202 Communicated by Charles G. Sibley, June 20, 1988 (receivedfor review April 7, 1988) ABSTRACT We obtained 5' and 3' flnking sequences (and not a monophyletic Pongidae). At present, the (5.4 kilobase pairs) from the *V-globin gene region of the human/African ape grouping remains the most widely ac- rhesus macaque (Macaca mulatta) and combined them with cepted hypothesis, as it is heavily supported by both available nucleotide data. The completed sequence, represent- DNA-DNA hybridization (13, 14) and nucleotide sequence ing 10.8 kilobase pairs of contiguous noncoding DNA, was (15) data. compared to the same orthologous regions available for human The P-globin gene family in catarrhine primates [humans, (Homo sapiens, as represented by five different alleles), com- great apes, and Old World monkeys (family Cercopitheci- mon chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), and dae)] has been well characterized in terms of its evolution, orangutan (Pongo pygmaeus). The nucleotide sequence for structure, and function (16). In catarrhines, this cluster Macaca mulatto provided the outgroup perspective needed to consists of six (3-related globin genes linked 5' to 3': E evaluate better the relationships of humans and great apes. (embryonic)-f-'y2 (fetal)-,qn (inactive pseudogene)-s- Pairwise comparisons and parsimony analysis of these ortho- l3(adult) (17). In this study, upstream and downstream flank- logues clearly demonstrated (i) that humans and great apes ing sequences of the 4rM-globin locus [an additional 5.4 share a high degree of genetic similarity and (a) that humans, kilobase pairs (kbp)] were determined for the rhesus macaque chimpanzees, and gorillas form a natural monophyletic group. (Macaca mulatta, family Cercopithecidae).** These se- These conclusions strongly favor a genealogical classification quences were combined with published nucleotide data (15, for higher primates consisting of a single family (Hominidae) 18) and then compared to orthologous regions available for with two subfamilies (Homininae for Homo, Pan, and Gorilla human (Homo sapiens, as represented by five alleles), and Ponginae for Pongo). common chimpanzee (Pan troglodytes), gorilla (Gorilla go- rilla), and orangutan (Pongo pygmaeus). These orthologues, Huxley (1) and Darwin (2) were the first to suggest that covering nearly 10.8 kbp, represented the longest contiguous African apes [represented then by the common chimpanzee stretch of noncoding DNA known for humans and other (Pan troglodytes) and the gorilla (Gorilla gorilla) and more higher primates (19). The completed sequence for rhesus recently as well by the pygmy chimpanzee (Pan paniscus)] macaque provided the outgroup perspective needed to eval- are the closest living relatives of humans (Homo sapiens). uate further the phylogenetic relationships and taxonomic The taxonomic importance of these observations was not affinities of higher primates (6-8). With this sequence, addressed by Huxley (1), as humans were assigned by him to extensive molecular evidence was obtained in favor of a their own suborder of Primates. In contrast, Darwin (2) genealogical classification for humans and great apes (20, 21). proposed that, from a genealogical perspective, humans should not occupy more than a unique subfamily or family. In the last century, most classifications for higher primates MATERIALS AND METHODS recognized separate families for humans and great apes: Nudeotide Sequences. Nucleotide sequence data from the Hominidae for humans and Pongidae for the African apes and *q-globingene region ofMacaca mulatta were obtained from orangutan (Pongo pygmaeus) of southeast Asia (i.e., refs. 3 the same pBR322 clone (pMmul4.7-R10.0) used by Koop et and 4). In these schemes, gibbons (Hylobates and Sympha- al. (15) and Slightom et al. (22). The same 5' and 3' flanking langus) were assigned to either their own family (Hyloba- sequences obtained by Miyamoto et al. (19) were determined tidae) or to that for the great apes (Pongidae). In the latter for this clone by the chemical sequencing method (23). The case, little doubt exists that the family Pongidae is rendered data obtained (5.4 kbp) were then combined with published unnatural [paraphyletic or polyphyletic (5)] by the inclusion 0/rr-gene sequences for rhesus macaque (15), thereby com- of these hominoid genera (6-8). Greater dispute surrounds pleting the same orthologous region (7.6 kbp) available for the genealogical affinities of the great apes themselves, and human, common chimpanzee, gorilla, and orangutan (19). as such, the monophyly of their family (Pongidae, restricted Adjacent sequences from further downstream [an additional hereafter to African and Asian apes). The morphological 3.2 kbp of 3' flanking DNA (18)] were added-to these 7.6-kbp studies of Schultz (9) and Kluge (10) support the existence of orthologues, thereby completing the 10.8-kbp alignment of a great ape clade (and therefore the monophyly ofPongidae). continuous noncoding DNA used in our analysis. In contrast, Schwartz (11, 12), using anatomical data, argues The nucleotide data base for humans consisted of five for separate human/orangutan and chimpanzee/gorilla lin- partial sequences representing different alleles of the 10.8- eages, whereas molecular data and other morphological kbp region. In all, two upstream and three downstream alleles evidence clearly favor a human/African ape arrangement tTo whom reprint requests should be addressed. The publication costs of this article were defrayed in part by page charge **The sequence reported in this paper is being deposited in the payment. This article must therefore be hereby marked "advertisement" EMBL/GenBank data base (IntelliGenetics, Mountain View, CA, in accordance with 18 U.S.C. §1734 solely to indicate this fact. and Eur. Mol. Biol. Lab., Heidelberg) (accession no. J03818). 7627 Downloaded by guest on September 28, 2021 7628 Evolution: Miyamnoto et al. Proc. Nati. Acad. Sci. USA 8S (1988) G AA G CA T C G T 120 A C G C G G A 240 Al'r IT C A cc 360 Oc C A G G A A C C 480 T G T CA G A G A C 600 C Tr' C ACAT 720 TWCAGT? G AMr T A C C A 840 C C G A GG C A 960 T T 113 7GGCGG~fGIII30AO 1080 ~~~~~ - ~~~~~~~~~~~~~~i'r ~~~~~~~~~~~~1200 ~~~ - - 1'!' GC'I'IGAG~~~~~~~~~~~~~~~~~~~~ 1320 ~CGCG------------ ITCA G T ATiTCT T T 1440 A-MOMOAGAMOA3 G CA C TA A T G 1560 CAW T AA A T CA G A * 1680 T **** C A 1920 T C C A A CA T 'TC 4200 G C G T G A A A CA A A GA 4320 * ~~~~~~~TG* C C 4440 C C T GG G A A 4560 AA G T T AG T 4680 G G G A G T T A 4800 A C A CIW'1AAGACAAAAITC T 4920 Tr' TG G G C C C 5040 G T AA Cr' G A T G 5160 CA A *T 5280 A CA C C T A T C G G G 5400 A G A A A G A 5520 ***TGACTCT ~T C C G G GT T 5640 T T A 5760 G C *** T T C 5880 T T CA A C C C C T G 6000 GrCCTT** GACAC A CA C 6120 G 0!' C C C C C G 6240 G G T C T 6360 A T A T A T Al'! GA T 6480 FIG. 1. (Figure continues on the opposite page.) Downloaded by guest on September 28, 2021 Evolution: Miyarnoto et aL Proc. Natl. Acad. Sci. USA 85 (1988) 7629 G C C A 'IT T 6600 TRAArA7CC4AAllAA=TAlTA(:CT C A T A AA 6720 T~rATMATAGGrAGA~Il'PCAXIC_LI"************************ A ATAXGr'aN'In1AAMt'I"Ir G ATG T 6840 A C C 6960 A G A C GC C TT A A 7080 * U G T A A A A *** ***********G T A A TG A A 7200 *~7AOAAA * CAG AT 7TG A* *I-rOLI#G C CCGNGAGAGAGAGAAG 7320 G CA T T G T ** 7440 A C T T A 7560 FIG. 1. Aligned DNA sequences of the 04ri-globin flanking regions for Homo sapiens and Macaca mulatta (upper and lower lines, respectively). Only nucleotides at variable sites for rhesus macaque and only regions corresponding to sequence obtained in this study are shown. The location ofthe Koop et al. (15) sequences is represented by the double row of + beginning after position 1999. The entire 10.8-kbp alignment is divided into upstream (positions 1-7556) and downstream (7551-10760) regions by the EcoRI site (7551-7556) signifying the start ofthe Maeda et al. (18) sequences. The human orthologue represented here is that of Collins and Weissman [CW (16)], as corrected by Miyamoto et al. (19). The nucleotide alignments of Koop et al. (15), Maeda et al. (18), and Miyamoto et al. (19) are followed in this study. To preserve the entire 10.8-kbp alignment, gaps (asterisks) are sometimes retained between human and rhesus macaque even in the absence of polymorphism (i.e., position 1555). All five species share an Alu repeat element with a downstream orientation at positions 1424-1756 (27). In contrast, a unique Ala repeat with an upstream orientation is exhibited by rhesus macaque at sites 1018-1334.
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