Phylogenetic relationships among Brazilian howler monkeys, genus Alouatta (Platyrrhini, Atelidae), based on <FONT FACE=Symbol>g</FONT>1-globin pseudogene sequences

gmb Genetics and Molecular Biology Genet. Mol. Biol. 1415-4757 1678-4685 Sociedade Brasileira de Genética Ribeirão Preto, SP, Brazil Os guaribas, do gênero Alouatta, que são os primatas do Novo Mundo com maior distribuição geográfica, têm sido colocados em três grupos de espécies: o grupo Alouatta palliata da América central, e os grupos sulamericanos Alouatta seniculus e Alouatta caraya. Este último é monotípico, mas o grupo A. seniculus inclui pelo menos três espécies (A. seniculus, A. belzebul e A. fusca). Neste estudo, foram seqüenciados aproximadamente 600 pares de base do pseudogene globina g1 nas quatro espécies brasileiras (A. seniculus, A. belzebul, A. fusca e A. caraya). Os métodos de máxima parcimônia e máxima verossimilhança produziram árvores filogenéticas com o mesmo arranjo: {A. caraya [A. seniculus (A. fusca, A. belzebul)]}. A árvore mais parcimoniosa apresentou valores de bootstrap maiores de 82% para todos os agrupamentos, e valores de força de ligação de pelo menos 2, apoiando o agrupamento irmão de A. fusca e A. belzebul. O estudo também confirmou a presença em A. fusca do elemento de inserção Alu, com 150 pares de base, e uma deleção de 1,8 kb no pseudogene globina g1 já conhecidos nas demais espécies de guaribas. A classificação cladística baseada em dados moleculares é congruente com as de estudos morfológicos, com um isolamento claro do grupo monoespecífico A. caraya em relação ao grupo A. seniculus. Phylogenetic relationships among Brazilian howler monkeys, genus Alouatta (Platyrrhini, Atelidae), based on g1-globin pseudogene sequences Carla Maria Meireles1, JohnCzelusniak1, Stephen F. Ferrari2, Maria Paula CruzSchneider2 and MorrisGoodman1 1Department of Anatomy and Cell Biology, Wayne State University School of Medicine, 550 East Canfield Ave. MRB 422, Detroit, MI 48201, USA. Send correspondence to C.M.M. Fax: [phone]. E-mail:[e-mail]. 2Departamento de Genética, CCB, Universidade Federal do Pará, Caixa Postal 8607, 66.075-900 Belém, PA, Brasil. ABSTRACT The genus Alouatta (howler monkeys) is the most widely distributed of New World primates, and has been arranged in three species groups: the Central American Alouatta palliata group and the South American Alouatta seniculus and Alouatta caraya groups. While the latter is monotypic, the A. seniculus group encompasses at least three species (A. seniculus, A. belzebul and A. fusca). In the present study, approximately 600 base pairs of the g1-globin pseudogene were sequenced in the four Brazilian species (A. seniculus, A. belzebul, A. fusca and A. caraya). Maximum parsimony and maximum likelihood methods yielded phylogenetic trees with the same arrangement: {A. caraya [A. seniculus (A. fusca, A. belzebul)]}. The most parsimonious tree had bootstrap values greater than 82% for all groupings, and strength of grouping values of at least 2, supporting the sister clade of A. fusca and A. belzebul. The study also confirmed the presence of a 150-base pair Alu insertion element and a 1.8-kb deletion in the g1-globin pseudogene in A. fusca, features found previously in the remaining three species. The cladistic classification based on molecular data agrees with those of morphological studies, with the monospecific A. caraya group being clearly differentiated from the A. seniculus group. INTRODUCTION The systematics of the New World monkeys (infraorder Platyrrhini) has undergone considerable revision during the past two decades, but remains controversial (e.g. Rosenberger, 1984; Ford, 1986; Kay, 1990). Nevertheless, recent studies of DNA sequences (Schneider et al., 1993, 1996; Harada et al., 1995; Goodman, 1996; Barroso et al., 1997) have consistently supported an arrangement which recognizes only 15 genera, distributed in three families: Atelidae, Pitheciidae and Cebidae. Following this arrangement, the Atelidae encompasses four genera: Alouatta (howler monkeys), Ateles (spider monkeys), Brachyteles (muriquis) and Lagothrix (woolly monkeys). Relationships within the ateline clade - Ateles, Brachyteles and Lagothrix - have been disputed, but there is a growing consensus on the grouping of Brachyteles and Lagothrix, including conclusive evidence from gamma(g)-globin gene sequences (Meireles et al., 1999). With one exception (Kay, 1990), there is also a general consensus on the distinct position of Alouatta, which is placed separately in either its own tribe, Alouattini (Rosenberger, 1984; Ford, 1986), or subfamily, Alouattinae (Hill, 1962; Napier and Napier, 1967; Hershkovitz, 1977). Alouatta is the most widely distributed Neotropical primate genus (Neville et al., 1988), ranging from southern Mexico to northern Argentina, and is found in tropical and subtropical forest ecosystems throughout Brazil (Hirsch et al., 1991). Hershkovitz (1949) recognized three species groups based on the structure of the hyoid apparatus: the Central American Alouatta palliata group, and the South American Alouatta seniculus and Alouatta caraya groups. While the latter group is monotypic, the other two encompass a variety of different forms, whose arrangement has been subject to conflicting interpretations (e.g. Hershkovitz, 1949; Hill, 1962; Mittermeier et al., 1988; Groves, 1993; Bonvicino et al., 1995; Stanyon et al., 1995; Rylands and Brandon-Jones, 1998). Despite the need for further work, especially on the integration of genetic and morphological data, the most recent major revisions of the genus (Hershkovitz, 1949; Hill, 1962) all divide the A. seniculus group into three species: A. seniculus, A. belzebul (endemic to Brazil) and A. (guariba) fusca. Groves (1993) does recognize a fourth species, Alouatta sara, but it is endemic to Bolivia, and thus not relevant to the present study. More recent studies (Bonvicino et al., 1995) also allocate species status to a number of subspecific forms of both A. seniculus and A. belzebul, but in the absence of a consensus, the arrangement of Groves (1993) will be followed here. In addition to other unresolved questions, the karyotype of Alouatta varies from 2n = 43 to 2n = 54 (Armada et al., 1987; Lima and Seuánez, 1991; Stanyon et al., 1995). Of the four Brazilian species, only A. caraya has a fixed number of chromosomes, with 2n = 52 (Pargament et al., 1984), whereas in A. seniculus, 2n varies from 43 to 49 (Yunis et al., 1976; Lima and Seuánez, 1991). A. belzebul and A. fusca, on the other hand, share both the same diploid number (2n = 49/50) and a translocation on the Y chromosome (Koiffmann and Saldanha, 1974; Armada et al., 1987). In humans, the g-globin gene is located on the short arm of chromosome 11 (Lebo et al., 1979; Bunn and Forget, 1986). This gene is expressed embryonically in strepsirrhine primates (Tagle et al., 1988), but was duplicated in tandem in anthropoids (g1 and g2), becoming expressed fetally (Fitch et al., 1991). This globin gene is part of the beta(b)-globin gene cluster, which in primates includes the e, g, yh, d and b globin genes (Figure 1). All genes in this cluster have three exons and two introns (Lawn et al., 1980). In the atelids, g1 is a pseudogene (Meireles et al., 1995, 1998), whereas in the platyrrhine genera Aotus and Saimiri, the two loci are combined into a hybrid gene (Chiu et al., 1996). Figure 1 - Model of the b-cluster showing the five globin genes. The g1-globin pseudogene is amplified exhibiting the primers R1 and R2 used in this study and also the 1.8-kb deletion shared by all four Alouatta species as well as by the ateline group (Meireles et al., 1995, 1998). Several recent studies (Schneider et al., 1993, 1996; Harada et al., 1995; Porter et al., 1995, 1997a,b; Meireles et al., 1999) have used DNA sequences of the globin gene to resolve phylogenetic relationships in the platyrrhines, producing results generally consistent with those of more traditional morphological studies in most (see Schneider and Rosenberger, 1996), but not all (Shoshani et al., 1996) cases. In the present study, sequences of the g1-globin pseudogene were used in a molecular analysis of the phylogenetic relationships among Brazilian howler monkeys. The aligned sequences were also used to estimate divergence times based on a local molecular clock, and to investigate the presence of the Alu insertion - found in other Alouatta species (Meireles et al., 1995, 1998) - in A. fusca. MATERIAL AND METHODS Study species Howler monkeys are large-bodied, prehensile-tailed platyrrhines more specialized for folivory than frugivory, as is typical of other atelids. They are also highly sexually dimorphic in body size (adult males are 70-80% heavier than females), and two of the Brazilian species (A. caraya and A. fusca) are among only three platyrrhines (the other is Pithecia pithecia) to exhibit sexual dimorphism in pelage coloration (Mittermeier et al., 1988). A. belzebul also exhibits the most marked individual variation in pelage coloration of any platyrrhine (Bonvicino et al., 1989). Only one species (A. belzebul) is endemic to Brazil, but it is also the only one found in both Amazonian and Atlantic forest biomes. The remaining three species are found in Amazonia (A. seniculus), the Brazilian Atlantic forest and neighboring areas (A. fusca), and the savanna and swampy habitats of central and western Brazil (A. caraya). Preparation and amplification of DNA Genomic DNA was extracted from the peripheral blood cells of captive specimens of the four Brazilian howler monkey species (Table I), and the g1-globin sequences for A. caraya, A. belzebul and A. seniculus were determined by C.M.M. (Meireles, 1997). DNA extraction for A. caraya and A. seniculus was based on the protocol of Bell et al. (1981), whereas for A. belzebul and A. fusca, that of Sambrook et al. (1989) was used. The g1 fragment was obtained using the PCR protocol described in Meireles et al. (1995), and consisted of an initial denaturation of 3 min at 94oC followed by 30 cycles of denaturation at 94oC (30 s), annealing at 55oC (45 s), extension at 72oC (45 s) and a final extension of 10 min at 72oC. The amplification products were separated by agarose gel electrophoresis. The DNA primers (synthesized at the Center for Molecular Medicine and Genetics, Wayne State University, Detroit, USA) were: R1 5' -AAT GTG GAA GAT GCT GGG- 3' and R2 5' -GTC ATG TCT GAG CAA CAA AC- 3' Despite the presence of a 1.8-kbg1 deletion in all four species (Figure 1), these primers amplified a ~600-bp fragment in all cases. Cloning of PCR products The PCR products were separated in 1.0% agarose gels in TBE buffer (89 mM Tris-base, 89 mM boric acid and 2 mM EDTA, pH 8.0) containing 0.5 mg ethidium bromide/ml. The amplified fragments were excised and purified using a Qiaex II gel extraction kit (Qiagen). The purified DNA fragments were cloned into the pGEM-T vector system I (Promega) and transformed into Escherichia coli host JM109 (Promega) according to the protocol supplied by the vendors. Single-stranded DNA was prepared from selected clones using helper phage M13K07 (Promega) and purified by PEG-NaCl precipitation followed by phenol-chloroform extraction and ethanol precipitation. Sequencing Nucleotide sequences were determined for at least three clones of each species by the dideoxy chain-termination method (Sanger et al., 1977) using a Sequenase version 1.0 kit (United States Biochemical). The sequences were aligned by eye using version 3.0 of the ESEE sequence editor (Cabot and Beckenbach, 1989). Gaps were inserted to minimize the number of nucleotide substitutions and indels (insertions/deletions) needed to account for the descent of the aligned sequences. As PCR reactions commonly result in slightly different sequences for the same cloned fragments, a consensus sequence of three or more clones was defined for each species. These consensus sequences were then aligned against the known orthologous sequences which represented the outgroups for the phylogenetic analysis: Cebus albifrons (Cal), Macaca mulatta (Mmu) and Homo sapiens (Hsa). Phylogenetic analysis Phylogenetic analyses were performed using the maximum parsimony and maximum likelihood methods. The most parsimonious and the maximum likelihood trees were determined using the phylogenetic analysis using parsimony (PAUP) parsimony program, version 4.0 for DOS (written by David Swofford, Smithsonian Institute, Washington, DC, USA). For both trees, the strength of grouping values or Bremer decay indices were estimated using the PAUP program, and bootstrap analysis was applied to test the support for each grouping. Two thousand bootstrap replications with one shuffle per replication were carried out on the seven data sets. The number of parsimony-informative characters (synapomorphies) was established by eye and confirmed by the PAUP program. Divergence times were estimated using the branch lengths of the maximum likelihood tree constructed from a distance matrix calculated using Kimura's (1980) model. The molecular clock was calibrated using the local clock procedure, based on Goodman's (1996) estimate of 21 MYA for the divergence between Cebus and Alouatta. RESULTS AND DISCUSSION Analysis of g 1-pseudogene sequences PCR amplification using the 5' R1 and 3' R2 primers produced two fragments for all four genera. The fragment corresponding to g1 contained approximately 600 bp, and that of g2 about 2100 bp (Figure 2). The sequences indicated that this difference in size was due to a ~1.8-kb deletion at the g1 locus, which is shared by all four atelid genera (Meireles et al. 1995, 1998). These authors also encountered a ~150-bp insertion, described as a monomeric Alu element by Drs. Roy Britten (CIT, Pasadena, USA) and Jerzy Jurka (UC, Berkeley, USA), in A. caraya, A. belzebul and A. seniculus. In the present study, this same 150-bp Alu insertion was also found in A. fusca, indicating that it is an important synapomorphic marker for the analysis of Alouatta phylogeny and evolution. Figure 2 also shows a clear difference in the size of the g 1-globin fragment in two representative atelid genera, Ateles (~450 bp) and Alouatta (~600 bp). Figure 2 - PCR-amplified g gene DNA in atelids: 1 - g1 fragment of the purified PCR product of Alouatta belzebul; 2 - g1 fragment of the purified PCR product of Ateles geoffroyi; 3 - g2 fragment of the purified PCR product of Alouatta caraya; 4 - PCR products of the genomic DNA of Alouatta caraya; 5 - 1-kb DNA ladder. The nucleotide sequences bordered by primers R1 and R2 in the seven primate species studied here spanned a total of 2,482 aligned base positions (Figure 3) consisting of the following g1 gene regions: the 5' coding region of exon 1 (1-35), intron 1 (36-160), exon 2 (161-211), a ~1.8-kb deletion (212-2092), a region between the deletion and insertion (2093-2149), a ~150-bp insertion (2150-2298), and the 3' flanking region (2299-2482). In the phylogenetic analysis, all sequences except that of A. fusca were also represented by a 1.8-kb region extending upstream from the R1 primer. The sequences in this region are described in Meireles et al. (1999). The DNA sequences were deposited in GenBank (Table I), and are also available from the authors on request, or can be accessed via internet at http://ns.med.wayne.edu/. Phylogeny of Brazilian howler monkeys The maximum parsimony consensus tree (Figure 4), constructed using the PAUP program, had a nucleotide substitution score of 813 (length). The numbers above the lines show the minimum number of additional substitutions required to break up the clade (strength of grouping - SOG - value or Bremer decay index), while the numbers below the lines show the bootstrap values (number of times the grouping was encountered in 2,000 replicates) as percentages. The arrangement of howler species was: {A. caraya [A. seniculus (A. fusca, A. belzebul)]}, with SOG values of 66, 2 and 2, respectively. Figure 4 - Maximum parsimony tree derived from the aligned g1-globin nucleotide sequences in seven simian species. The length, or nucleotide substitution score, is 813. Values above the lines represent the minimum number of additional substitutions required to break up the clade designated by that node and those below the lines, the percentage of bootstrap values obtained in 2,000 replicates. All bootstrap values were greater than the critical value of 75% proposed by Hillis and Bull (1993), with a minimum value of 82% for the A. seniculus-A. belzebul/A. fusca clade. The A. belzebul-A. fusca clade was supported by a value of 88%, while 100% of the replications identified A. caraya as the basal species. The number of shared-derived sequence changes (synapomorphies) found by the PAUP analysis also supported this arrangement. The positions of the synapomorphies for the Alouatta species clades (Figure 3) were: A. fusca x A. belzebul - 48 (G®A), 77 (C®G), 79 (G®A) with homoplasy and 2318 (A®C) with homoplasy; Alouatta species - 212 (C®1.8-kb deletion), 2095 (del®A), 2096 (del®G), 2117 (T®G), 2145 (G®T), 2150 (del®150-bp Alu insertion), 2324 (C®T) with homoplasy, 2335 (C®T), 2349 (C®G), 2401 (G®A), 2403 (G®A), 2405 (G®A), 2411 (G®A), 2416 (A®del) and 2451 (C®T). The natural logarithm (ln) of the likelihood for the best maximum likelihood tree using the aligned g-globin sequences was -9329.13944. Bootstrap values (as a percentage of 2,000 replicates) are shown below the lines (Figure 5). Although the topologies of the tree and bootstrap values for the first (88) and last (100) clades were the same, the A. seniculus-A. belzebul/A. fusca clade had a borderline bootstrap value of 72. This analysis confirmed the cladistic groupings shown by the maximum parsimony tree (Figure 4). Figure 5 - Maximum likelihood tree derived from the aligned g1-globin nucleotide sequences in seven simian species. Log likelihood is -9329.13944. Values above the lines represent the minimum decrease in the log likelihood required to break up the clade designated by that node and those below the lines, the percentage of bootstrap values obtained in 2,000 replicates. Although the A. belzebul-A. fusca clade was relatively well defined, with a high bootstrap value (88%) and four shared synapomorphies, the analysis did not permit identification of the species closest to A. seniculus, despite the relative geographic proximity of A. belzebul in southwestern Amazonia (Hirsch et al., 1991). The data, nevertheless, supported the presence of a well-defined A. seniculus group [A. seniculus (A. belzebul, A. fusca)] as proposed by Hershkovitz (1949) and still widely accepted (e.g. Mittermeier et al., 1988). There is little doubt from these data that A. caraya should be placed in a distinct, monotypic group, and that Alouatta is monophyletic, with 15 synapomorphies. The divergence times between the different Alouatta lineages (Table II) were calculated by the local molecular clock method, based on Goodman's (1996) estimate of 21 MYA for the split between Alouatta and Cebus, using the maximum likelihood branch lengths for the sequences of the g1-globin pseudogene. This analysis indicated that the different Alouatta lineages diverged relatively recently in relation to the putative + 11 MYA split of the alouattine and ateline groups (Meireles et al., 1999). Overall, then, the results of the present study corroborate the phylogenetic relationships among Brazilian howler monkey species suggested by morphological characteristics (Mittermeier et al., 1988), principally the existence of distinct A. caraya and A. seniculus groups, which diverged approximately 2.5 MYA (Table II). ACKNOWLEDGMENTS We thank Dr. Kathy Neiswanger (University of Pittsburgh Medical Center, Pittsburgh, PA, USA), Adelmar Coimbra-Filho and Alcides Pissinatti (Centro de Primatologia do Rio de Janeiro, RJ, Brazil), and José A.P.C. Muniz (Centro Nacional de Primatas, Ananindeua, PA, Brazil) for the samples used in this study. We also thank Drs. Roy Britten (California Institute of Technology, Pasadena) and Jerzy Jurka (University of California, Berkeley) for classifying the monomeric Alu insertion of 150 bp found in the Alouatta sequences. This research was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil (No. 201530/93-7), National Institutes of Health (NIH), USA (No. HL33940) and the National Science Foundation (NSF), USA (No. DEB9116098). RESUMO Os guaribas, do gênero Alouatta, que são os primatas do Novo Mundo com maior distribuição geográfica, têm sido colocados em três grupos de espécies: o grupo Alouatta palliata da América central, e os grupos sulamericanos Alouatta seniculus e Alouatta caraya. Este último é monotípico, mas o grupo A. seniculus inclui pelo menos três espécies (A. seniculus, A. belzebul e A. fusca). Neste estudo, foram seqüenciados aproximadamente 600 pares de base do pseudogene globina g1 nas quatro espécies brasileiras (A. seniculus, A. belzebul, A. fusca e A. caraya). Os métodos de máxima parcimônia e máxima verossimilhança produziram árvores filogenéticas com o mesmo arranjo: {A. caraya [A. seniculus (A. fusca, A. belzebul)]}. A árvore mais parcimoniosa apresentou valores de bootstrap maiores de 82% para todos os agrupamentos, e valores de força de ligação de pelo menos 2, apoiando o agrupamento irmão de A. fusca e A. belzebul. O estudo também confirmou a presença em A. fusca do elemento de inserção Alu, com 150 pares de base, e uma deleção de 1,8 kb no pseudogene globina g1 já conhecidos nas demais espécies de guaribas. A classificação cladística baseada em dados moleculares é congruente com as de estudos morfológicos, com um isolamento claro do grupo monoespecífico A. caraya em relação ao grupo A. seniculus. (Received September 3, 1998) Armada, J.L.A., Barroso, C.M.L., Lima, M.M.C., Muniz, J.A.P.C. and Seuánez, H.N. (1987). Chromosome studies in Alouatta belzebul. Am. J. Primatol. 13: 283-296. Chromosome studies in Alouatta belzebul Am. J. Primatol. 1987 283 296 13 Armada J.L.A. Barroso C.M.L. Lima M.M.C. Muniz J.A.P.C. Seuánez H.N. Bailey, W.J., Hayasaka, K., Skinner, C.G., Kehoe, S., Sieu, L.C., Slightom, J.L. and Goodman, M. (1992). Reexamination of the African hominoid trichotomy with additional sequences from the primate b-globin gene cluster. Mol. Phylogenet. Evol. 1: 97-135. Reexamination of the African hominoid trichotomy with additional sequences from the primate <FONT FACE="Symbol">b</FONT>-globin gene cluster Mol. Phylogenet. Evol. 1992 97 135 1 Bailey W.J. Hayasaka K. Skinner C.G. Kehoe S. Sieu L.C. Slightom J.L. Goodman M. Barroso, C.M.L., Schneider, H., Schneider, M.P.C., Sampaio, I., Harada, M.L., Czelusniak, J. and Goodman, M. (1997). Update on the phylogenetic systematics of New World monkeys: further DNA evidence for placing the pygmy marmoset (Cebuella) within the genus Callithrix. Int. J. Primatol. 18: 651-674. Update on the phylogenetic systematics of New World monkeys: further DNA evidence for placing the pygmy marmoset (Cebuella) within the genus Callithrix Int. J. Primatol. 1997 651 674 18 Barroso C.M.L. Schneider H. Schneider M.P.C. Sampaio I. Harada M.L. Czelusniak J. Goodman M. Bell, G.I., Karam, J.H. and Rutter, W.J. (1981). Polymorphic DNA region adjacent to the 5' end of the human insulin gene. Proc. Natl. Acad. Sci. USA 78: 5759-5763. Polymorphic DNA region adjacent to the 5' end of the human insulin gene Proc. Natl. Acad. Sci. USA 1981 5759 5763 78 Bell G.I. Karam J.H. Rutter W.J. Bonvicino, C.R., Langguth, A. and Mittermeier, R.A. (1989). A study of the pelage color and geographic distribution in Alouatta belzebul (Primates, Cebidae). Rev. Nordestina Biol. 6: 139-148. A study of the pelage color and geographic distribution in Alouatta belzebul (Primates, Cebidae) Rev. Nordestina Biol. 1989 139 148 6 Bonvicino C.R. Langguth A. Mittermeier R.A. Bonvicino, C.R., Fernandes, M.E.B. and Seuánez, H.N. (1995). Morphological analysis of Alouatta seniculus species group (Primates, Cebidae). A comparison with biochemical and karyological data. Hum. Evol. 10: 169-176. Morphological analysis of Alouatta seniculus species group (Primates, Cebidae): A comparison with biochemical and karyological data Hum. Evol. 1995 169 176 10 Bonvicino C.R. Fernandes M.E.B. Seuánez H.N. Bunn, H.F. and Forget, B.G. (1986). Hemoglobin: Molecular, Genetic and Clinical Aspects. W.B. Saunders Company, Philadelphia. Hemoglobin: Molecular, Genetic and Clinical Aspects 1986 Bunn H.F. Forget B.G. Cabot, E.L. and Beckenbach, A.T. (1989). Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Comput. Appl. Biosci. 5: 233-234. Simultaneous editing of multiple nucleic acid and protein sequences with ESEE Comput. Appl. Biosci. 1989 233 234 5 Cabot E.L. Beckenbach A.T. Chiu, C.-H., Schneider, H., Schneider, M.P.C., Sampaio, I., Meireles, C.M., Slightom, J.L., Gumucio, D.L. and Goodman, M. (1996). Reduction of two functional g-globin genes to one: an evolutionary trend in New World monkeys (Infraorder Platyrrhini). Proc. Natl. Acad. Sci. USA 93: 6510-6515. Reduction of two functional <FONT FACE="Symbol">g</FONT>-globin genes to one: an evolutionary trend in New World monkeys (Infraorder Platyrrhini) Proc. Natl. Acad. Sci. USA 1996 6510 6515 93 Chiu C.-H. Schneider H. Schneider M.P.C. Sampaio I. Meireles C.M. Slightom J.L. Gumucio D.L. Goodman M. Fitch, D.H.A., Bailey, W.J., Tagle, D.A., Goodman, M., Sieu, L. and Slightom, J.L. (1991). Duplication of the g-globin gene mediated by L1 long interspersed repetitive elements in an early ancestor of simian primates. Proc. Natl. Acad. Sci. USA 88: 7396-7400. Duplication of the <FONT FACE="Symbol">g</FONT>-globin gene mediated by L1 long interspersed repetitive elements in an early ancestor of simian primates Proc. Natl. Acad. Sci. USA 1991 7396 7400 88 Fitch D.H.A. Bailey W.J. Tagle D.A. Goodman M. Sieu L. Slightom J.L. Ford, S.M. (1986). Systematics of the New World monkeys. In: Comparative Primate Biology. Vol. 1. Systematics, Evolution, and Anatomy (Swindler, D.R. and Erwin, J., eds.). A.R. Liss, New York, pp. 73-135. Comparative Primate Biology: Vol. 1. Systematics, Evolution, and Anatomy 1986 73 135 Ford S.M. Swindler D.R. Erwin J. Goodman, M. (1996). Epilogue: a personal account of the origins of a new paradigm. Mol. Phylogenet. Evol. 5: 269-285. Epilogue: a personal account of the origins of a new paradigm Mol. Phylogenet. Evol. 1996 269 285 5 Goodman M. Groves, C.P. (1993). Order Primates. In: Mammal Species of the World: a Taxonomic and Geographic Reference (Wilson, D.E. and Reeder, D.M., eds.). Smithsonian Institution Press, Washington D.C., pp. 243-277. Mammal Species of the World: a Taxonomic and Geographic Reference 1993 243 277 Groves C.P. Wilson D. E. Reeder D.M. Harada, M.L., Schneider, H., Schneider, M.P.C., Sampaio, I., Czelusniak, J. and Goodman, M. (1995). DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes. Mol. Phylogenet. Evol. 4: 331-349. DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes Mol. Phylogenet. Evol. 1995 331 349 4 Harada M.L. Schneider H. Schneider M.P.C. Sampaio I. Czelusniak J. Goodman M. Hayasaka, K., Skinner, C.G., Goodman, M. and Slightom, J.L. (1993). The g-globin genes and their flanking sequences in primates: findings with nucleotide sequences of capuchin monkey and tarsier. Genomics 18: 20-28. The <FONT FACE="Symbol">g</FONT>-globin genes and their flanking sequences in primates: findings with nucleotide sequences of capuchin monkey and tarsier Genomics 1993 20 28 18 Hayasaka K. Skinner C.G. Goodman M. Slightom J.L. Hershkovitz, P. (1949). Mammals of northern Colombia. Preliminary report No. 4: monkeys (Primates), with taxonomic revisions of some forms. Proc. U.S. Nat. Mus. 98: 323-427. Mammals of northern Colombia: Preliminary report No. 4: monkeys (Primates), with taxonomic revisions of some forms Proc. U.S. Nat. Mus. 1949 323 427 98 Hershkovitz P. Hershkovitz, P. (1977). Living New World Monkeys (Platyrrhini) with an Introduction to Primates. Vol. I. University of Chicago Press, Chicago. Living New World Monkeys (Platyrrhini) with an Introduction to Primates 1977 Hershkovitz P. Hill, W.C.O. (1962). Primates, Comparative Anatomy and Taxonomy. Vol. V. Cebidae. Part B. University Press, Edinburgh. Primates, Comparative Anatomy and Taxonomy 1962 Hill W.C.O. Cebidae. Part B Hillis, D.M. and Bull, J.J. (1993). An empirical test of bootstrapping as a method of assessing confidence on phylogenetic analysis. Syst. Biol. 42: 182-192. An empirical test of bootstrapping as a method of assessing confidence on phylogenetic analysis Syst. Biol. 1993 182 192 42 Hillis D.M. Bull J.J. Hirsch, A., Landau, E.C., Tedeschi, A.C.M. and Menegheti, J.O. (1991). Estudo comparativo das espécies do genero Alouatta Lacépčde, 1799 (Platyrrhini, Atelidae) e sua distribuiçăo geográfica na América do Sul. In: A Primatologia no Brasil. Vol. 3 (Rylands, A.B. and Bernardes, T.A., eds.). Fundaçăo Biodiversitas, Belo Horizonte, pp. 239-262. A Primatologia no Brasil 1991 239 262 Hirsch A. Landau E.C. Tedeschi A.C.M. Menegheti J.O. Rylands A.B. Bernardes T.A. Kay, R.F. (1990). The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea). J. Hum. Evol. 19: 175-208. The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea) J. Hum. Evol. 1990 175 208 19 Kay R.F. Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J. Mol. Evol.16: 111-120. A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences J. Mol. Evol. 1980 111 120 16 Kimura M. Koiffmann, C.P. and Saldanha, P.H. (1974). Cytogenetics of Brazilian monkeys. J. Hum. Evol. 3: 275-282. Cytogenetics of Brazilian monkeys J. Hum. Evol. 1974 275 282 3 Koiffmann C.P. Saldanha P.H. Lawn, R.M., Efstratiadis, A., O'Connell, C. and Maniatis, T. (1980). The nucleotide sequence of the human b-globin gene. Cell 21: 647-651. The nucleotide sequence of the human <FONT FACE="Symbol">b</FONT>-globin gene Cell 1980 647 651 21 Lawn R.M. Efstratiadis A. O'Connell C. Maniatis T. Lebo, R.V., Carrano, A.V., Burkhart-Schultz, K., Dozy, A.M., Yu, L.C. and Kan, Y.W. (1979). Assignment of the human b-, g-, and d-globin genes to the short arm of chromosome 11 by chromosome sorting and DNA restriction enzyme analysis. Proc. Natl. Acad. Sci. USA 76: 5804-5808. Assignment of the human <FONT FACE="Symbol">b</FONT>-, <FONT FACE="Symbol">g</FONT>-, and <FONT FACE="Symbol">d</FONT>-globin genes to the short arm of chromosome 11 by chromosome sorting and DNA restriction enzyme analysis Proc. Natl. Acad. Sci. USA 1979 5804 5808 76 Lebo R.V. Carrano A.V. Burkhart-Schultz K. Dozy A.M. Yu L.C. Kan Y.W. Lima, M.M.C. and Seuánez, H.N. (1991). Chromosome studies in the red howler monkey, Alouatta seniculus stramineus (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex chromosome system and karyological comparisons with other subspecies. Cytogenet. Cell Genet. 57: 151-156. Chromosome studies in the red howler monkey, Alouatta seniculus stramineus (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex chromosome system and karyological comparisons with other subspecies Cytogenet. Cell Genet. 1991 151 156 57 Lima M.M.C. Seuánez H.N. Meireles, C.M. (1997). Molecular evolution of gamma 1 and gamma 2 globin genes in atelines (Primates, Platyrrhini). PhD thesis, Universidade Federal do Pará, PA, Brasil. Molecular evolution of gamma 1 and gamma 2 globin genes in atelines (Primates, Platyrrhini) 1997 Meireles C.M. Meireles, C.M., Schneider, M.P.C., Sampaio, M.I.C., Schneider, H., Slightom, J.L., Chiu, C.-H., Neiswanger, K., Gumucio, D.L., Czelusniak, J. and Goodman, M. (1995). Fate of a redundant g-globin gene in the atelid clade of New World monkeys: implications concerning fetal globin gene expression. Proc. Natl. Acad. Sci. USA 92: 2607-2611. Fate of a redundant <FONT FACE="Symbol">g</FONT>-globin gene in the atelid clade of New World monkeys: implications concerning fetal globin gene expression Proc. Natl. Acad. Sci. USA 1995 2607 2611 92 Meireles C.M. Schneider M.P.C. Sampaio M.I.C. Schneider H. Slightom J.L. Chiu C.-H. Neiswanger K. Gumucio D.L. Czelusniak J. Goodman M. Meireles, C.M., Czelusniak, J., Schneider, M.P.C. and Goodman, M. (1998). Hemoglobina fetal: estrutura, expressăo e evoluçăo do gene gama em primatas (Primates, Platyrrhini). In: Série Monografias No. 6 (Duarte, F.A.M., ed.). Sociedade Brasileira de Genética, Ribeirăo Preto, pp. 1-27. Série Monografias No. 6 1998 1 27 Meireles C.M. Czelusniak J. Schneider M.P.C. Goodman M. Duarte F.A.M. Meireles, C.M., Czelusniak, J., Schneider, M.P.C., Muniz, J.A.P.C., Brigido, M.C., Ferreira, H.S. and Goodman, M. (1999). Molecular phylogeny of ateline New World monkeys (Platyrrhini, Atelinae) based on g-globin gene sequences: evidence that Brachyteles is the sister group of Lagothrix. Mol. Phylogenet. Evol. 12: 10-30. Molecular phylogeny of ateline New World monkeys (Platyrrhini, Atelinae) based on <FONT FACE="Symbol">g</FONT>-globin gene sequences: evidence that Brachyteles is the sister group of Lagothrix Mol. Phylogenet. Evol. 1999 10 30 12 Meireles C.M. Czelusniak J. Schneider M.P.C. Muniz J.A.P.C. Brigido M.C. Ferreira H.S. Goodman M. Mittermeier, R.A., Rylands, A.B. and Coimbra-Filho, A.F. (1988). Systematics: species and subspecies - an update. In: Ecology and Behavior of Neotropical Primates. Vol. 2 (Mittermeier, R.A., Rylands, A.B., Coimbra-Filho, A.F. and da Fonseca, G.A.B., eds.). World Wildlife Fund, Washington D.C., pp. 13-75. Ecology and Behavior of Neotropical Primates 1988 13 75 Mittermeier R.A. Rylands A.B. Coimbra-Filho A.F. Mittermeier R.A. Rylands A.B. Coimbra-Filho A. F. da Fonseca G.A.B. Napier, J.R. and Napier, P.H. (1967). A Handbook of Living Primates. Academic Press, New York. A Handbook of Living Primates 1967 Napier J.R. Napier P.H. Neville, M.K., Glander, K.E., Braza, F. and Rylands, A.B. (1988). The howling monkeys, genus Alouatta. In: Ecology and Behavior of Neotropical Primates. Vol. 2 (Mittermeier, R.A., Rylands, A.B., Coimbra-Filho, A.F. and da Fonseca, G.A.B., eds.). World Wildlife Fund, Washington D.C., pp. 349-453. Ecology and Behavior of Neotropical Primates 1988 349 453 Neville M.K. Glander K.E. Braza F. Rylands A.B. Mittermeier R.A. Rylands A.B. Coimbra-Filho A.F. da Fonseca G.A.B. Pargament, M.D.M., Vinuesa, M.L.L., Colillas, O.J. and Salum, S.B. (1984). Banding patterns of Alouatta caraya. Rev. Bras. Genét. VII: 373-379. Banding patterns of Alouatta caraya Rev. Bras. Genét. 1984 373 379 VII Pargament M.D.M. Vinuesa M.L.L. Colillas O.J. Salum S.B. Porter, C.A., Sampaio, I., Schneider, H., Schneider, M.P.C., Czelusniak, J. and Goodman, M. (1995). Evidence on primate phylogeny from e-globin gene sequences and flanking regions. J. Mol. Evol. 40: 30-55. Evidence on primate phylogeny from e-globin gene sequences and flanking regions J. Mol. Evol. 1995 30 55 40 Porter C.A. Sampaio I. Schneider H. Schneider M.P.C. Czelusniak J. Goodman M. Porter, C.A., Czelusniak, J., Schneider, H., Schneider, M.P.C., Sampaio, I. and Goodman, M. (1997a). Sequences of the primate e-globin gene: implications for systematics of the marmosets and other New World primates. Gene 205: 59-71. Sequences of the primate <FONT FACE="Symbol">e</FONT>-globin gene: implications for systematics of the marmosets and other New World primates Gene 1997 59 71 205 Porter C.A. Czelusniak J. Schneider H. Schneider M.P.C. Sampaio I. Goodman M. Porter, C.A., Page, S.L., Czelusniak, J., Schneider, H., Schneider, M.P.C., Sampaio, I. and Goodman, M. (1997b). Phylogeny and evolution of selected primates as determined by sequences of the e-globin locus and 5' flanking regions. Int. J. Primatol. 18: 261-295. Phylogeny and evolution of selected primates as determined by sequences of the <FONT FACE="Symbol">e</FONT>-globin locus and 5' flanking regions Int. J. Primatol. 1997 261 295 18 Porter C.A. Page S.L. Czelusniak J. Schneider H. Schneider M.P.C. Sampaio I. Goodman M. Rogan, P.K., Pan, J. and Weissman, S.M. (1987). L1 repeat elements in the human e-Gg-globin gene intergenic region: sequence analysis and concerted evolution within this family. Mol. Biol. Evol. 4: 327-342. L1 repeat elements in the human <FONT FACE="Symbol">e</FONT>-G<FONT FACE="Symbol">g</FONT>-globin gene intergenic region: sequence analysis and concerted evolution within this family Mol. Biol. Evol. 1987 327 342 4 Rogan P.K. Pan J. Weissman S.M. Rosenberger, A.L. (1984). Fossil New World monkeys dispute the molecular clock. J. Hum. Evol. 13: 737-742. Fossil New World monkeys dispute the molecular clock J. Hum. Evol. 1984 737 742 13 Rosenberger A.L. Rylands, A.B. and Brandon-Jones, D. (1998). Scientific nomenclature of the red howlers from the northeastern Amazon in Brazil, Venezuela, and the Guianas. Int. J. Primatol. 19: 879-905. Scientific nomenclature of the red howlers from the northeastern Amazon in Brazil, Venezuela, and the Guianas Int. J. Primatol. 1998 879 905 19 Rylands A.B. Brandon-Jones D. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. Molecular Cloning: A Laboratory Manual 1989 Sambrook J. Fritsch E.F. Maniatis T. Sanger, F., Nicklen, S. and Coulson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463-5467. DNA sequencing with chain-terminating inhibitors Proc. Natl. Acad. Sci. USA 1977 5463 5467 74 Sanger F. Nicklen S. Coulson A.R. Schneider, H. and Rosenberger, A.L. (1996). Molecules, morphology, and platyrrhine systematics. In: Adaptive Radiations of Neotropical Primates (Norconk, M.A., Rosenberger, A.L. and Garber, P.A., eds.). Plenum Press, New York, pp. 3-19. Adaptive Radiations of Neotropical Primates 1996 3 19 Schneider H. Rosenberger A.L. Norconk M. A. Rosenberger A.L. Garber P.A. Schneider, H., Schneider, M.P.C., Sampaio, I., Harada, M.L., Stanhope, M., Czelusniak, J. and Goodman, M. (1993). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol. Phylogenet. Evol. 2: 225-242. Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) Mol. Phylogenet. Evol. 1993 225 242 2 Schneider H. Schneider M.P.C. Sampaio I. Harada M.L. Stanhope M. Czelusniak J. Goodman M. Schneider, H., Sampaio, I., Harada, M.L., Barroso, C.M.L., Schneider, M.P.C., Czelusniak, J. and Goodman, M. (1996). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron 1 and e-globin sequences. Am. J. Phys. Anthropol. 100: 153-179. Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP intron 1 and <FONT FACE="Symbol">e</FONT>-globin sequences Am. J. Phys. Anthropol. 1996 153 179 100 Schneider H. Sampaio I. Harada M.L. Barroso C.M.L. Schneider M.P.C. Czelusniak J. Goodman M. Shen, S.-H., Slightom, J.L. and Smithies, O. (1981). A history of the human fetal globin gene duplication. Cell 26: 191-203. A history of the human fetal globin gene duplication Cell 1981 191 203 26 Shen S.-H. Slightom J.L. Smithies O. Shoshani, J., Groves, C.P., Simons, E.L. and Gunnell, G.F. (1996). Primate phylogeny: morphological vs. molecular results. Mol. Phylogenet. Evol. 5: 102-154. Primate phylogeny: morphological vs. molecular results Mol. Phylogenet. Evol. 1996 102 154 5 Shoshani J. Groves C.P. Simons E.L. Gunnell G.F. Slightom, J.L., Blechl, A.E. and Smithies, O. (1980). Human fetal Gg- and Ag- globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell 21: 627-638. Human fetal G<FONT FACE="Symbol">g</FONT>- and A<FONT FACE="Symbol">g</FONT>- globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes Cell 1980 627 638 21 Slightom J.L. Blechl A.E. Smithies O. Slightom, J.L., Koop, B.F., Xu, P. and Goodman, M. (1988). Rhesus fetal globin genes: concerted gene evolution in the descent of higher primates. J. Biol. Chem. 263: 12427-12438. Rhesus fetal globin genes: concerted gene evolution in the descent of higher primates J. Biol. Chem. 1988 12427 12438 263 Slightom J.L. Koop B.F. Xu P. Goodman M. Stanyon, R., Tofanelli, S., Morescalchi, M.A., Agoramoorthy, G., Ryder, O.A. and Weinberg, J. (1995). Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus, Linnaeus) subspecies. Am. J. Primatol. 35: 171-183. Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus, Linnaeus) subspecies Am. J. Primatol. 1995 171 183 35 Stanyon R. Tofanelli S. Morescalchi M.A. Agoramoorthy G. Ryder O.A. Weinberg J. Tagle, D.A., Koop, B.F., Goodman, M., Slightom, J.L., Hess, D.L. and Jones, R.T. (1988). Embryonic e and g globin genes of a prosimian primate (Galago crassicaudatus): nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J. Mol. Biol. 203: 439-455. Embryonic e and g globin genes of a prosimian primate (Galago crassicaudatus): nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints J. Mol. Biol. 1988 439 455 203 Tagle D.A. Koop B.F. Goodman M. Slightom J.L. Hess D.L. Jones R.T. Yunis, E.J., Caballero, O.M.T., Ramirez, C. and Ramirez, Z.E. (1976). Chromosomal variation in the primate Alouatta seniculus seniculus. Folia Primatol. 25: 215-224. Chromosomal variation in the primate Alouatta seniculus seniculus Folia Primatol. 1976 215 224 25 Yunis E.J. Caballero O.M.T. Ramirez C. Ramirez Z.E.