Review Sheet for CHEM 257A at UA
Review Sheet for CHEM 257A at UA
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Nucleotide Sequence Analysis of the Lemur BGlobin Gene Family Evidence for Major Rate Fluctuations in Globin Polypeptide Evolution1 Stephen Harrisquotquot2 Justin R T hackeray Alec J Je reys and Mark L WeissT Department of Genetics University of Leicester and TDepartment of Anthropology Wayne State University Lemur Brelated globin genes have been isolated and sequenced Orthology of pro simian and human 8 7 and Brelated globin genes was established by dotmatrix analysis All of these lemur globin genes potentially encode functional B related globin polypeptides though precisely when the y globin gene is expressed remains unknown The organization of the l8kb brown lemur B globin gene cluster 5 e yqm51B 339 is consistent with its evolution by contraction via unequal crossing over from the putative ancestral mammalian B globin gene cluster 5 8Y115B 339 The dwarf lemur nonadult globin genes are arranged as in the brown lemur Similar levels of synonymous silent nucleotide substitutions and noncoding DNA sequence differences have accumulated between species in all of these genes suggesting a uniform rate of noncoding DNA divergence throughout primate B globin gene clusters These differences are comparable with those observed in the nonfunctional W11 pseudogene and have therefore accumulated at the presumably maximal neutral rate In contrast nonsynonymous replacement nucleotide substitutions show a significant heterogeneity in distribution for both the same gene in different lineages and different genes in the same lineage These major uctuations in replacement but not silent substitution rates cannot be attributed to changes in mutation rate suggesting that changes in the rate of globin polypeptide evolution in primates is not governed solely by variable mutation rates Introduction The regulated expression of the vertebrate a and B globin gene clusters results in the synthesis of several different forms of hemoglobin at different stages of devel opment The Bglobin gene cluster has been well characterized in a number of species from different mammalian orders for review see Collins and Weissman 1984 Pri mates have been studied in the greatest detail to reveal the possible evolutionary events that led to contemporary cluster organizations in this lineage Efstratiadis et a1 1980 Zimmer et a1 1980 Barrie et a1 1981 Martin et a1 1983 Harris et a1 1984 1 Scott et a1 1984 The human Bglobin gene cluster consists of ve active genes and a pseudogene arranged in the order 5 eGyAywnSJB 339 Efstratiadis et a1 1980 Fritsch et a1 1980 This arrangement of the Bglobin gene cluster appears stable in evolution in that a 1 Key words prosimian Bglobin genes adult and nonadult globin genes nucleotide substitution rates rabbit anthropoids humans 2 Current address Animal Breeding Research Organization Edinburgh Address for correspondence and reprints Dr Mark L Weiss Department of Anthropology Wayne State University Detroit Michigan 48202 Mol Biol Evol 36465 484 1986 1986 by The University of Chicago All rights reserved 0737403886030636050200 465 466 Harris Thackeray Jetfreys and Weiss similar cluster arrangement is found in the great apes and oldworld m0nkeys whose common ancestor occurred 20 40 Myr ago Barrie et a1 1981 In contrast the owl monkey Aotus trivirgatus a newworld monkey and several lemurs prosimians all have shorter B globin gene clusters Barrie et a 1981 The owl monkey B globin gene cluster is arranged 5 e y tlmSB 3 Harris et a1 1984 and the brown lemur cluster contains single 8 7 and Brelated globin genes plus a hybrid lmSglobin pseudogene Barrie et a1 1981 Jeffreys et a1 1982 Harris et a1 1984 The ancestral primate B globin gene cluster was probably arranged 5 e ywn 83 3 as still exists in the owl monkey Harris et a1 1984 During primate evolution several events have therefore resulted in alterations in Bglobin gene cluster arrange ment The duplication giving rise to the G7 and A39yglobin genes of oldworld monkeys apes and man probably occurred after the separation of catarrhines and platyrrhines Barrie et a1 1981 Shen et a1 1981 along with an expansion of the 87 intergenic region possibly caused by the insertion of two Kpn like repetitive elements Forget et a1 1981 reviewed in Karlsson and Nienhuis 1985 In lemurs the ancestral cluster contracted through an unequal exchange between the um pseudogene and the neigh boring Bglobin gene resulting in a hybrid wnSglobin pseudogene Jeffreys et a1 1982 Harris et a1 1984 In man the aglobin gene is expressed during embryogenesis the 07 and A7 globin genes during later fetal development and the 5 minor and 3 major adult genes from late gestation onward reviewed in Collins and Weissman 1984 Similarly in other nonprimate mammals rabbit mouse goat and cow orthologues of e and B globin genes are also expressed during embryonic and adult and fetal in goat and cow development respectively Hardies et a1 1984 Hardison 1984 Hill et a1 1984 Townes et a1 1984 Schimenti and Duncan 1985 In contrast minor adult 8like globin chains are only found in man apes and newworld monkeys Boyer et a1 1969 1971 orthologues of 8 having been silenced in the remaining primate groups oldworld monkeys Kimura and Tagaki 1983 Martin et a1 1983 and lemurs J e reys et a1 1982 Harris et a1 1984 and in other nonprimate mammals rabbit Hardison and Margot 1984 and mouse Hardies et a1 1984 Fetal 39yglobin chains are only found in higher primates orthologues of the 39y globin gene in other mammals rabbit Hardison 1981 and mouse Hill et a1 1984 being expressed during early embryogenesis The 39yglobin gene has therefore apparently switched from embryonic to fetal expression during primate evolution Fetal globin chains have been found in newworld monkeys Huisman et a1 1973 and other higher primates but there is no evidence for a fetal hemoglobin containing ylike globin chains in prosimian neonate blood Buettner Janusch et a1 1972 Therefore it is possible that the prosimian yrelated globin gene is expressed during embryonic de velopment along with presumably the erelated globin gene Alternatively the pro simian y related gene andor the erelated gene may be nonfunctional pseudogenes To establish the evolutionary orthology and functional potentials of the prosimian 8 7 and Brelated globin genes the Bglobin gene cluster has been isolated from the brown lemur Lemur macaco fulvus mayottensis and the region encompassing the 8 and 39ylike globin genes has been isolated from another distantly related prosimian the dwarf lemur Cheirogaleus medias Sequence analysis of these genes con rms their orthology to the human 8 7 and B globin genes and shows that they have the potential to encode Blike globin polypeptides Detailed DNA sequence comparisons show that noncoding DNA differences and silent site substitutions have occurred to similar extents in different genes and lineages but replacement site substitutions show Lemur BGlobin Genes 467 a signi cant heterogeneity in their distribution This might have resulted from sub stantial accelerations of speci c protein evolution in some lineages accelerations that are not attributable to an increased mutation rate Material and Methods Preparation of DNA and Genomic Cloning DNA was prepared from the liver of a brown lemur Lemur macaco fulvus mayottensis and the whole carcass of a dwarf lemur Cheirogaleus medius J e reys 1979 Dwarf lemur and brown lemur genomic DNA libraries were constructed in the bacteriophage vector MA7 1 Loenen and Brammar 198039 Je reys et al 1982 and screened for Bglobin DNA sequences by hybridization with 32P labeled rabbit adult Bglobin cDNA Maniatis et a1 1976 DNA Sequencing A DNA fragment containing the brown lemur B globin gene was subcloned into pAT153 Twigg and Sherratt 1980 mapped by the method of Smith and Birnstiel 1976 and sequenced by the method of Maxam and Gilbert 1977 1980 The dwarf lemur y globin gene and brown lemur 8 and yglobin genes were subcloned into pUCl3 Messing 1983 and sequenced by the dideoxynucleotide chaintermination method Sanger et al 1977 Biggin et al 1983 Sequencing data were assembled with the aid of computer programs developed by Staden 1980 All genes were completely sequenced on both strands DNA Sequence Analysis and Determination of Branch Lengths of Phylogenetic Trees DNA sequences were aligned by computergenerated dot matrices White et al 1984 to identify the positions of insertionsdeletions Final alignments were carried out by eye Sequence differences between aligned human lemur and rabbit genes were partitioned onto an unrooted threebranch phylogenetic tree by the maximum parsimony minimumsubstitution criterion The majority of differences 86 were each unique to one of the three species and could therefore be placed unambiguously on one branch of the tree The remaining positions which differed in all three species were scored as two substitutions These substitutions were partitioned to branches of the tree using the unambiguous substitution branch lengths If the three branches A B and C carried a b and c unambiguous substitutions respectively then the prob ability of substitutions on A and B but not on C resulting in an ambiguous position is given by aba ba b c3 The relative probability that the ambiguous sub stitutions at a given site are on branches AB rather than on BC or AC is therefore aba baba b bcb c aca c Since substitutions on AB or AC each increase the branch length of A by one the probability that an ambiguous position includes a substitution on A is aba b ada caba b bcb c aca c Thus each ambiguous substitution was partitioned onto the tree in the ratio aba b aca caba b bcb cada c bcb c onto branches A B and C respectively For more complex trees the very small number of ambiguous substitutions were partitioned similarly For exon sequences the phy logenetic distribution of most ambiguous replacement and silent substitutions could be resolved by reference to Brelated globin gene sequences of additional species goat Schon et al 1981 Shapiro et al 1983 and mouse Konkel et a1 1979 Hansen et a1 1982 Hill et al 1984 In the few instances in which a substitution could be either 476 Harris Thackeray Jeffreys and Weiss Weissman 1984 This places the initial 131 5bp duplication at gt200 Myr ago before the diversi cation of the Blike globin genes Efstratiadis et a1 1980 The retention of an identi able repeatunit structure in this region over such a considerable time presumably re ects its close proximity to the transcriptionally important 80 region of globin genes Moschonas et al 1982 Dierks et al 1983 Uniform Noncoding DNA Sequence Evolution in the Primate B Globin Gene Cluster The divergence of noncoding DNA sequences between homologous brown lemur and human um pseudogenes has previously been established as 028 substitutions per nucleotide site corrected for multiple substitutions Harris et al 1984 A similar degree of sequence divergence is also observed between homologous noncoding DNA sequences of the 8 7 and B globin genes 025 035 and 032 respectively corrected for multiple substitutions with no signi cant differences in the levels of divergence of intron 1 intron 2 and 3 anking DNA results not shown This suggests that noncoding DNA sequences in these functional genes are evolving at or close to the maximal neutral rate Assuming the anthropoidprosimian divergence to have occurred some 60 Myr ago Barrie et al 1981 we observed that the noncoding DNA sequence divergence corresponds to an average rate of 25 X 10 9 substitutions per site per year over several regions of the primate Bglobin gene cluster This substitution rate for noncoding DNA sequences in the primate Bglobin gene cluster is substantially less than the supposedly constant rate of mammalian noncoding DNA evolution a rate that is based on primaterodent and primate lagomorph gene comparisons 5 X 10 9 substitutions per site per year Hayashida and Miyata 1983 This discrepancy may re ect lineagespeci c differences in nucleotide substitution rate as has been suggested by the comparison of rodent and human sequences Wu and Li 1985 Noncoding DNA sequences and pseudogenes in par ticular have been proposed as paradigms of neutral evolution Li et al 1981 Kimura 1983 Therefore a substitution rate of 25 X 10 9 per site per year may more accurately re ect the underlying average neutral mutation rate Operating on the Beglobin gene cluster in the primates see Chang and Slightom 1984 Goodman et al 1984 Harris et al 1984 for further discussion Timing of the CheirogaleidaeLemuridae Divergence Although a phylogeny for the major prosimian primate groups is generally ac cepted Martin 1972 Eaglen 1983 Schwartz and Tattersall 1985 the sparse and incomplete fossil record has frustrated attempts to accurately establish species diver gences with respect to an evolutionary time scale For example it is unclear whether the dwarf lemUr is more closely related to Lorisidae and Galagidae or instead to Le muridae prosimians see Schwartz and Tattersall 1985 Assuming a clocklike rate of noncoding DNA change in different primate lineages of 25 X 10 9 substitutions per site per year the 009 substitutions per site corrected for multiple substitutions ob served between noncoding regions of brown lemur and dwarf lemur y globin gene sequences suggests that these species diverged 18 Myr ago see also g 5 This is much more recent than would be expected on the basis of nonmolecular data which suggests that the prosimian radiation began some 55 Myr ago Schwartz and Tattersall 1985 This discrepancy casts doubts either on the timing of the prosimian radiation or on the grouping of the Cheirogaleidae represented by the dwarf lemur with the prosimian families Lorisidae and Galagidae rather than with the Lemuridae Schwartz and Tattersall 1985 Lemur B Globin Genes 477 e 397 6 H513 qu NC 8 R NC S R NC 8 R a b 119 125 119 217 171 75 a 114 39 w 147 144 140 74 39175 95 175 39 93 as 1 59 177 45 150 272 b 91 123 111 1 1 112 i 53 137 50 137 15 c 245 105 r 333 15 7 130 03 c 198 220 221 241 127 27 1 i 143 272 144 x 03 33 50 161 70 545 Ocu S B Obs Exp Hsa Age qu Cme 55 75 d e 1 g 75 33 54 75 03 40 97 1 20 104 320 293 Ocu X 396 FIG 5 Unrooted tree analysis of DNA sequence substitutions accumulated within Brelated globin genes A Base differences between human Hsa brown lemur qu and rabbit Gen 8 y or B globin genes were determined from the alignments shown in gs 2 4 and were partitioned onto different branches of an unrooted phylogenetic tree as described in Material and Methods Percentages of noncoding DNA changes NC on each branch were determined from intron 1 intron 2 and 3 anking sequences the conserved 5 anking region Moschonas et a1 1982 the 10 bp immediately adjacent to the 5 and 3 splice sites and the 3 nontranslated region were excluded Within coding DNA two classes of base substitution were scored the actual number of replacement substitutions R observedexpected and the number of silent or synonymous codon changes S observedexpected The expected number of silent substitutions was calculated from the noncoding DNA branch lengths the best estimate of the level of neutral substitutions in each lineage assuming no selection against silent substitutions and that 28 of all codingsequence substitutions are silent determined by computer simulation of codingsequence evolution that allowed for a high level 65 of transitions as estimated from noncoding DNA changes The expected number of 39 replacement substitutions were similarly estimated on the further assumption that a constant proportion f0 of replacement substitutions are selectively neutral f0 0205 for B globin based on Kimura 1983 Deviations from expectation over the entire tree were determined by the 76 test Yates s correction 3 df Individual branches that gave rise to signi cant deviations are indicated by crosshatching 005 gt P gt 001 stippling 001 gt P gt 0001 and solid shading 0001 gt P B Further partitioning of primate and rabbit yglobin gene differences onto an unrooted phylogenetic tree Additional species included are the newworld monkey Ateles geo royi Age Giebel et a1 1985 and the prosimian Cheirogaleus medius Cme present paper Comparative Analysis of DNA Sequence Evolution in Different BcGlobin Genes and Mammalian Lineages Having established alignments for the functional orthologues of human brown lemur and rabbit 8 y and Bglobin genes gs 2 4 we partitioned DNA sequence differences within each gene onto branches of an unrooted phylogenetic tree g 5A 478 Harris Thackeray Jeffreys and Weiss thereby allowing subsequent detailed comparisons of DNA sequence evolution within different lineages and regions of different functional genes Noncoding DNA Sequence Evolution Homologous noncoding DNA sequences introns and 3 anking DNA have diverged to similar extents along each branch of the unrooted tree in all genes g 5A There is however a signi cant tendency 001 gt P gt 0001 for orthologues of the e globin gene to evolve some 10 20 slower than B or 7 along all branches of the tree possibly owing to some additional functional constraint or localized reduction in mutation rate acting on the noncoding regions of the eglobin gene In addition when rabbit noncoding DNA sequences are used as an outgroup there is a consistent asymmetry between human and lemur branch lengths in all trees 005 gt P gt 001 the lemur branch having accumulated some 20 fewer changes than the human branch A similar asymmetry in branch lengths between Malagasy prosimians and other primate groups has been observed by Bonner et a1 1980 suggesting that there may have been a general deceleration in DNA evolution in Malagasy primates relative to that in other primates Silent Substitutions in Coding Sequences Assuming that the observed noncoding DNA sequence differences represent the maximum potential neutral change along a given branch it is possible to calculate the expected number of silent substitutions that should have accumulated on each branch for a given gene see legend to g 5 The resulting ratio of the observed to expected number of silent substitutions provides an estimate of the proportion f0 of silent changes that are selectively neutral f0 1 if there is no selection against silent substitutions Kimura 1983 The mean ratio of observedexpected silent substitutions on all branches of all three trees corresponds to f0 091 With the possible exception of the rabbit branch of the B globin tree which has accumulated fewer silent substi tutions than expected 001 gt P gt 0001 f0 047 there is therefore no strong evidence for any substantial selection against silent substitutions in these functional primate Bglobin genes This contrasts with the apparent selection against synonymous codon substitutions in functional genes observed by Miyata and Hayashida 1981 f0 05 comparing noncoding DNA substitution rate to synonymous codon substi tution rate which they attributed to biases in synonymous codon utilization see also Kimura 1983 Replacement Substitutions in Coding Sequences If a constant proportion of potential replacement substitutions are selectively neutral f0 0205 for B globin based on Kimura 1983 it is also possible to calculate the expected number of replacement substitutions for a given noncoding branch length see legend to g 5 The number of replacement substitutions on each branch of the eglobin tree do not deviate signi cantly from expectation g 5A however the observed replacement substitutions on both the y and Bglobin trees show major deviations from expectation with a larger than expected number of observed changes in the human branch of the 39yglobin tree and in the brown lemur branch of the 3 globin tree This heterogeneity in replacement substitutions is in accord with the observations of Langley and Fitch 1974 who noted a signi cant nonuniformity in rate of amino acid substitution both in the same protein in different lines of descent and among Lemur BGlobin Genes 479 different proteins in the same line of descent The fact that heterogeneity in branch lengths is gene speci c and furthermore is speci c to replacement and not silent substitutions suggests that these deviations are not the result of a general change in mutation rate on different branches but rather represent a speci c alteration in the number of replacement substitutions in a given gene Accelerated y Globin Gene Evolution in Early Anthropoids To investigate further the distribution of replacement substitutions in the 39y globin gene during anthropoid evolution sequence comparisons were extended to include the 39yglobin sequences of the dwarf lemur and the spider monkey Ateles geo royi a newworld monkey g 5B Signi cantly larger than expected numbers of replacement substitutions have accumulated on at least two branches of the anthropoid tree branches e and h g 5B This is particularly pronounced on branch h leading from the anthropoidprosimian divergence to the catarrhineplatyrrhine divergence Inter estingly this correSponds to the epoch in which the ancestral primate yglobin gene may have been recruited from an embryonic to a fetal stage of developmental expres sion Adaptive evolution occurring as embryonic 39y globin altered to ll its new fetal role is therefore an attractive explanation for the accelerated level of replacement but not silent substitutions on this branch of the tree Alterations at those amino acid positions affecting 23diphosphoglycerate binding and therefore oxygen af nity may have been particularly important for the fetal role of yglobin Bunn 1980 Goodman 1981 However most 19 of 29 of the replacement substitutions have occurred at positions of unknown functional signi cance and it is possible that many or all of these additional replacement substitutions may have arisen from an increase in the proportion of acceptable neutral replacement substitutions during for example a period of reduced selective constraint f0 gt 0205 The pro portion of the expected number of replacement substitutions that have accumulated on branch h f0 06 ie still lt1 is consistent for example with a model in which the 39yglobin gene was completely silenced f0 1 for a period of some 12 Myr prior to reactivation and adoption as a fetal globin gene The observed heterogeneity in replacement substitutions on different branches of the anthropoid y globin tree is therefore not inconsistent with the neutral theory provided that the 39yglobin gene has passed through epochs of weak or absent selective constraint The duplicated y globin loci in higher primates have apparently been involved in several rounds of inter39y gene conversion Slightom et a1 1980 Scott et a1 1984 However conversions of the y globin gene by nonyglobin genes is unlikely to have resulted in the observed number of replacement substitutions in the y globin genes There is no evidence for either replacement substitutions being clustered within the gene or any increase in silent substitutions as might be expected as the result of a substantial intergenic conversion However it is not possible to discount small ran dom sequence microconversions as a source of some of the replacement substitutions in this gene see below Accelerated Evolution of the Brown Lemur BGlobin Gene The unrooted B globin replacement substitution tree shows a signi cant excess of replacement substitutions in the brown lemur lineage P lt 0001 g 5A It is di icult to assess the in vivo physiological signi cance if any of these substitutions and therefore dif cult to attribute a dominant role to adaptive evolution in their xation Similarly the ratio of observedexpected replacement substitutions in this 480 Harris Thackeray Jeffreys and Weiss lineage corresponding to f0 077 is high for a functional B globin gene especially since the B globin gene being the only functional adult B globin gene locus in the cluster is unlikely to have been silenced at any time during brown lemur evolution It is therefore unlikely though not inconceivable f0 still lt1 that the high level of replacement substitutions in this lineage has accumulated solely as a result of neutral drift in a protein that for a long period has been largely free of selective constraint Many ll of 26 of the observed replacement substitutions occur in the rst 13 codons of the rst exon Similar numbers of amino acid differences in this region have previously been noted in other lemuroid B globin chains Hill and BuettnerJanusch 1964 Coppenhaver et a1 1983 but not in another group of related prosimians the lorises Maita et a1 1978 It is possible that intergenic gene conversion involving another Blike globin gene of the brown lemur cluster may have led to such a clustering of substitutions in this gene This is an attractive mechanism since the donor 3 like globin sequence is itself likely to be compatible with continued function of the adult B globin gene However there is no apparent B globin related donor sequence in the contemporary brown lemur B globin gene cluster results not shown Harris 1985 One possible explanation for this is that this region was converted by the ancestral lemur 5like gene prior to the unequal exchange that gave rise to the hybrid wn pseudogene Harris et a1 1984 However in the absence of a genuine ancestral 5 globin sequence all mammalian orthologues of 8 having been involved in recombi national exchanges with other members usually adult of the B globin gene cluster this possibility cannot be tested Another possibility is that this region has undergone a microconversion by a moderately similar random region of the brown lemur genome perhaps by recombination mechanisms involved in chromosome pairing during meiosis see Smithies and Powers 1986 Comparing the rst 13 codons of the brown lemur and human B globin genes 17 differences in 39 nucleotides it can be estimated that there may be 105 microdonors in the brown lemur genome any one of which could have converted this region of the B globin gene However a single such microconversion event could account for neither the elevated level of replacement substitutions found throughout the brown lemur Bglobin gene nor the apparent lack of a correspondingly enhanced level of silent substitutions nor the elevated level of replacement substitutions observed on more than one branch of the anthropoid y globin tree see above Conclusion The DNA sequences presented herein complete the characterization of B related loci in the brown lemur Bglobin gene cluster While DNA sequence analysis con rms the orthology and functional potential of nonadult lemur B globin genes DNA se quence comparisons alone cannot determine when these genes are expressed during development The apparent absence of a fetal hemoglobin containing y like chains BuettnerJanusch et a1 1972 suggests that the lemur y globin gene is expressed during embryogenesis as is the case in rabbit and mouse and that the recruitment to fetal development occurred after anthropoids diverged from prosimians some 60 Myr ago Comparative DNA sequence analysis has shown a uniformity in the level of noncoding DNA sequence divergence and silent substitution over the entire B globin gene cluster a uniformity that is probably close to or at the maximal neutral sub stitution rate in the primate phylogeny In contrast replacement substitutions are extremely heterogeneous in their distribution varying between genes in the same Icmur B Globin Genes 481 lineage and for the same gene in different lineages This signi cant variation in rate of replacement substitution although in some cases possibly a result of adaptive evo lution or gene conversion is not necessarily inconsistent with the neutral theory of evolution Acknowledgments Our thanks to Victoria Wilson for excellent technical assistance and Dr John F Y Brook eld for advice on statistical analysis We are also grateful to Lynne Walters Jersey Wildlife Preservation Trust the Duke University Primate Center and Dr M Goodman Wayne State University for generous donations of primate tissue This work was supported by a grant to AJJ from the Medical Research Council and by grants to MW from the National Science Foundation BNS 823077 and the Wenner Gren Foundation for Anthropological Research AJJ is a Lister Institute Research Fellow LITERATURE CITED BARALLE F C SHOULDERS S GOODBOURN A JEFFREYS and N PROUDFOOT 1980a The 5 anking region of the human aglobin gene Nucleic Acids Res 84393 4404 BARALLE F C SHOULDERS and N PROUDFOOT 1980b The primary structure of the human auglobin gene Cell 21621 626 BARRIE P A JEFFREYS and A SCOTT 1981 Evolution of the B globin gene cluster in man and the primates J Mol Biol 149319 336 BIGGIN M T GIBSON and H HONG 1983 Buffer gradient gels and 358 label as an aid to rapid DNA sequence determination Proc Natl Acad Sci USA 803963 3965 BONNER T R HEINEMANN and G TODARO 1980 Evolution has been retarded in Malagasy primates Nature 286420 423 BOYER S E CROSBY A NOYES G FULLER S 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