Primate Evolution at the DNA Level

8/7/2019 Primate Evolution at the DNA Level

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J Mol Evol (1990) 30:260-266J o u r n a l o fM o l e c u la r E v o l u t io n@ Springer-Verlag New York Inc. 1990

P r i m a t e E v o l u t i o n a t t h e D N A L e v e l a n d a C l a s s i f i c a t i o n o f H o m i n o i d s

Morris Go odm an, 1 Danilo A. Tagle, 2 Dav id H.A. Fitch, 1 Wen dy Bailey, e Jo hn Czelusniak, 1Ben F. Koop, 2. Philip Benson, 1 and Jerry L. Sl ightom L3

Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, Michigan 48201, USA2 Department of Molecular Biology and Genetics, Wayne State University School of Medicine, Detroit, Michigan 48201, USA

3 Division of Molecular Biology, The Upjohn Company, Kalamazoo, Michigan 49007, USA

S u m m a r y. The genetic distances among primatelineages estimated fro m orthologous noncodin g nu-cleotide sequences o f ~-type globin loci and theirflanking and intergenic DNA agree closely with th edistances (delta TsoH values) esti mated by cross hy-bridization of total genomic single-copy DNAs.These DNA distances and the maxi mum parsimonytree constructed for the nucleotide sequence ortho-logues depict a branching pat tern of prima te lineagesthat is essentially congruent with the picture fromphylogenetic analyses of morphological characters.The molecular evidence, however, resolves ambi-guities in the morphological picture and providesan objective view of the cladistic position of human samong the primates. Th e molecular data group hu-mans with chimpanzees in subtribe Homini na, withgorillas in tribe Hominin i, orangutans in subfamilyHomininae, gibbons in family Hominidae, OldWorld monkeys in infraorder Catarrhini, New Worldmonkeys in semisubo rder Anthropoidea, tarsiers in

suborder Haplorhini, and strepsirhines (lemuri-forms and lorisiforms) in order Primates. A seemingincongruency between organismal and molecularlevels of evolution, namely t hat morphological evo-lution appears to have speeded up in higher pri-mates, especially in the lineage to humans, whilemolecular evolution has slowed down, may havethe trivial explanatio n that relatively small geneticchanges may sometimes result in marked pheno-typic changes.

* C u r r e n t a d d r e s s : Division of Biology, Califomia Institute ofTechnology, Pasadena, California 91125, USAO f f p r i n t r e q u e s t s t o :M. Goodman

Key words: Nonc odin g nucleot ide sequences --DNA hybridization -- Primate phylogeny -- Max-imu m pars imony -- Cladistic classification

In t roduc t ion

The Linnaean system of taxonomic classification,by virtue of its hierarchical ranks for nested taxa,provides a formal nomenclatur e or vocabulary thatis well suited for describing the cladistic relation-ships that exist among species. Ever since Darwin(1859) proposed that taxonomic classif icat ionsshould group species according to their recency ofcommon ancestry, research in systematics has be-come increasingly concerned with identifyingmonophyletic groups or clades and with revisingtraditional t axonomic classifications so that they re-flect the cladistic hypotheses best supported by the

data. When revisions are now proposed they areusually in the direction of having taxa representclades instead of grades, the latter being ra ther ar-bitrary groupings for species with pri miti ve featuresof morphology or for species with advanced featuresof morp holo gy (Simpson 1961). Progress toward aconsisten tly cladistic classification for the primat eshas been impeded by ambiguities in the morpho-logical picture o f primate phylogeny and by an an-thropocentric view of nature that persists. As ex-pressed in extreme form in pre-Darwinian t axono my,this anthropocentric view placed humans on a ped-

estal between the animals and the angels in a king-dom all to ourselves. In modern taxonomy the an-thropocentric view is expressed by the gradisticdivision of the order Primates into suborder Pro-


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s imi i f o r t he sma l l -b r a ined p r ima te s (g roup ingi n f r a o r d e r s L e m u r i f o r m e s , L o r i s i f o r m e s , a n d Ta r -s i if o r m e s) a n d s u b o r d e r A n t h r o p o i d e a f o r t h e l a rg e -b r a i n e d p r i m a t e s ( g r o u p i n g s u p e r f a m i l ie s C e b o i d e a ,C e r c o p i t h e c o i d e a , a n d H o m i n o i d e a ) a n d f u r t h e r b yt h e g r a d i st i c d i v i s io n o f H o m i n o i d e a i n t o a n a p ef a m i ly P o n g i d a e fo r t h e n o n h u m a n h o m i n o i d s ( th e

fos si l apes and t he l i v ing g ibbons , o r angu tan s , go -r il la s, a n d c h i m p a n z e e s ) a n d a h u m a n f a m i l y H o -m i n i d a e f o r h u m a n s a l o n e .

P h y l o g e n e t i c a n a l y s e s o f m o r p h o l o g i c a l f e a t u re si n d i c a t e t h a t L e m u r i f o r m e s a n d L o r i s i f o r m e s a r es i s t e r g roups ( c lo se s t l i v ing r e l a t i ve s ) bu t d i s ag reeo n w h e t h e r t h e d w a r f a n d m o u s e l e m u r s ( C h e i ro -g a le i d ae ) b e l o n g w i t h o t h e r M a l a g a s y l e m u r s i n L e -m u r i f o r m e s o r in L o r i s i f o r m e s w i t h t h e A f r ic a n g a -l agos and po t to s and As i an l o r i s e s ( s ee F leag l e 1988f o r r e v ie w ) . M o r e o v e r, t h e s e m o r p h o l o g i c a l s t u d i esd o n o t u n a m b i g u o u s l y e s t a b l i s h t h e c l a d i s t i c p o s i -t i o n o f t h e Ta r s i i f o rm e s , w h i c h i n c l u d e s t h e P h i l -i p p i n e a n d I n d o n e s i a n t a r si e rs i n t h e g e n u sTarsiusa s t h e o n l y l i v i n g r e p r e s e n t a t i v e s o f th i s a n c i e n tp r i m a t e c l ad e . A w i d e l y h e l d v i e w i s t h a t P r i m a t e sd i v i d e s c l a d i s t ic a l l y i n to S t r e p s i r h i n i ( L e m u r i -f o r m e s a n d L o r i s i f o r m e s ) a n d H a p l o r h i n i ( Ta r s i -i f o r m e s a n d A n t h r o p o i d e a ) ( A i e ll o 1 9 8 6 ; F le a g l e1 9 8 8) , b u t S i m o n s a n d R a s m u s s e n ( 1 9 8 9 ) c h a ll e n g et h is v i e w. T h e m o r p h o l o g i c a l e v i d e n c e d i v i d e s A n -t h r o p o i d e a i n t o i n f ra o r d e r s P l a t y r r h i n i f o r c e b o i d s( th e N e w W o r l d m o n k e y s ) a n d C a t a r r h i n i f o r c er -

c o p i t h e c o i d s ( t h e O l d Wo r l d m o n k e y s ) a n d h o m i -n o i d s . T h e m o r p h o l o g i c a l e v i d e n c e a l s o i n d i c a t e st h a t H o m i n o i d e a d i v i d e s i n t o a g i b b o n o r le s s er a p ec l a d e a n d a g r e a t a p e - h u m a n c l a d e c o n t a i n i n go rangu tans , go r i l l a s , ch impanzees , and humans , bu th a s n o t u n a m b i g u o u s l y r e s o l v e d t h e b r a n c h i n g p a t -t e r n o f t h e g re a t a p e - h u m a n c l ad e .

I n re c e n t p a p e r s ( G o o d m a n e t a l. 1 9 8 9 ; K o o p e ta l. 1 9 8 9) w e h a v e s h o w n t h a t t h e g e n e t i c re c o r d o fe v o l u t io n i n D N A p r o v i d e s a v ie w o f p r i m a t e p h y -l o g e n y t h a t i s e s s e n t i a l l y c o n g r u e n t w i t h t h e m o r -p h o l o g i c a l e v i d e n c e . T h e m o l e c u l a r d a t a , h o w e v e r,r e so lve amb igu i t i e s i n t he morpho log i ca l p i c tu r e andp r o v i d e a n o b j e c t i v e v i e w o f t h e c l a d is t ic p o s i t i o no f h u m a n s a m o n g t h e a p e s . U s i n g a v a i l a b l e s e -que nce da ta on the 13-type g lo bin loc i (~, 3", ~ , 6 , /3)a n d t h e i r f l a n k i n g a n d i n t e rg e n i c D N A f r o m p r i -m a t e s a n d o t h e r m a m m a l s , w e a li g ne d o r t h o lo g o u sn u c l e o t i d e s e q u e n c e s a n d c o n s t r u c t e d m o s t p a r s i -m o n i o u s t r e e s f r o m t h e a l i g n e d o r t h o l o g u e s . T h es e q u e n c e d a t a f o r t h e C h e i r o g a l e id a e c o n s i s t e d o f a2 0 0 0 - b a s e s e q u e n c e s p a n n i n g t h e d w a r f l e m u r ' s7 - g l o b i n l o c u s , a n d t h e m a x i m u m p a r s i m o n y t r e e

c o n s t r u c t e d f o r 3 "- g lo b in o r t h o l o g u e s s t r o n g l yg r o u p e d d w a r f l e m u r w i t h b r o w n l e m u r ( a l e m u ri d )r a the r t han w i th ga l ago , i nd i ca t i ng t ha t Che i roga l -e i d a e b e l o n g s i n L e m u r i f o r m e s a n d n o t i n L o r i s i -

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fo rmes (Tag le e t a l . 1988 ; Koop e t a l . 1989 ) . Thes e q u e n c e d a t a f o rTarsius w e r e m o r e t h a n f iv e t i m e sg rea te r, cons i s t i ng o f nuc l e o t i de s eq uence s spann ingeac h o f the f ive 13-type loci , a nd the ~, 3 ', ~b~, 6, and/3 m a x i m u m p a r s i m o n y t r e es a ll c o n g r u e n t ly p l a c e dTa r s i i f o r m e s i n s u b o r d e r H a p l o r h i n i a s t h e s i s t e rg r o u p o f A n t h r o p o i d e a ( n o w t r e a te d t a x o n o m i c a l l y

a s a s e m i s u b o r d e r ) ; i n t u r n , L e m u r i f o r m e s ( r e p r e -sen t ed by a l l fi ve l oc i i n t he ca se o f b ro wn l emur )and Lor i s i fo rm es ( r ep re sen t ed by ga l ago e and 3" l oc i)w e r e s i st e r g r o u p s t h a t j o i n e d t o g e t h e r t o f o r m s u b -o rde r S t r eps i rh in i (Koop e t a l . 1989 ) .

To r e s o l v e t h e b ra n c h i n g p a t t e r n o f t h e g r e a t a p e -h u m a n c l ad e , w e ( G o o d m a n e t al . 1 9 8 9; K o o p e ta l . 1989 ) combined nuc l eo t i de s equenc ing r e su l t sf r o m s e v e r a l st u d i es ( K o o p e t a l. 1 9 8 6; M i y a m o t oe t a l . 1987, 1988; F i tch e t a l . 1988; Maeda e t a l .1988 ) . These combined r e su l t s gave u s a da t a s e t o fa l i gned hum an , ch im panzee , go r i ll a , o r angu tan , r he -s u s m o n k e y, a n d s p i d e r m o n k e y o r t h o l o g u e s . E a c ho r t h o l o g u e r e p r e s e n t e d 1 0.8 k b o f c o n t i n u o u s n o n -cod ing se que nce s ta r t ing up s t rea m of the ~b~7-globinl o c u s a n d e n d i n g d o w n s t r e a m o f i t b e f o r e r e a c h i n gt h e 6 l oc u s. T h e m a x i m u m p a r s i m o n y a n d m a x i -m um l i ke l i hood t ree s cons t ruc t ed u s ing t he se a l i gnedo r t h o l o g u e s p r o v i d e d o v e r w h e l m i n g e v i d e n c e f o rt h e s e p a r a t io n o f o r a n g u t a n f r o m a m o n o p h y l e t i ch u m a n - c h i m p a n z e e - g o r i l l a b r a n ch a n d , t o g e th e rw i t h o t h e r D N A s t u d ie s (S i b le y a n d A h l q u i s t 1 9 8 4 ,1 9 8 7 ; H o l m q u i s t e t a l . 1 9 8 8 ; C a c c o n e a n d P o w e l l

1 9 8 9; U e d a e t a l. 1 9 8 9 ; Wi l l i a m s a n d G o o d m a n1989) , s i gn i f i can t ev idence t ha t human and ch im-p a n z e e l i n e a g e s s h a r e d t h e m o s t r e c e n t c o m m o nances to r.

Sa r i ch e t a l . ( 1989 ) , i n c r i t i c i z ing t he DNA hy-b r i d i z a t i o n d a t a o f S i b le y a n d A h l q u i s t ( 1 9 8 4 , 1 9 8 7 )and Bonne r e t a l . ( 1980 ) , c l a imed tha t t he se hy -b r i d i z a t i o n d a t a d i d n o t a c c u r a t e ly m e a s u r e t h e d i s -t a n c e s a m o n g o r t h o l o g o u s p r i m a t e D N A s . Ye t t h eD N A h y b r i d iz a t i o n d i s t an c e s r e p o rt e d b y S i b l e y a n dAhlq u i s t ( 1987 ) fo r c a t a r rh ines an d by Bo nn e r e t a l.( 1 9 8 0 ) f o r m o r e a n c i e n t l y s e p a r a t e d p r i m a t e l i n -eages ag ree c lo se ly w i th t he d i s t ances t ha t we fo undo n c o m p a r i n g o r t h o l o g o u s n o n c o d i n g s e q u e n c e sf rom in t ron , f l ank ing , and i n t e rgen i c r eg ions o f ther - t y p e g l o b in l oc i o f d i ff e re n t p r i m a t e s ( K o o p e t a l.1989 ). I n th i s pape r, we i nc rea se t he se com par i son sm a i n l y w i t h ( 1) o r th o l o g o u s g i b b o n s e q u e n c e s ( F i t c he t a l. 1989 ; F i t ch , Ba i ley, S l i gh tom, an d G oo dm an ,u n p u b l i s h e d d a t a) , t h e r e b y h a v i n g a l l f iv e m a j o rh o m i n o i d l i n e a g e s r e p r e s e n t e d , a n d ( 2 ) a d d i t i o n a lo r tho logous ga l ago s equences , more d i s t a l 5 ' f l ank -i n g 3' s e q u e n c e a n d t h e n o n c o d i n g s e q u e n c e f r o m a

ga l ago t 3 -g lob in l ocus (Tag le , Benson , and Good-m a n , u n p u b l i s h e d d a t a ) b e i n g a d d e d t o t h a t p r e v i -ous ly pu b l i shed fo r ga l ago ~ and 3" l oc i (Tag l e e t a l .1988 ). Fu r the r, we ma tch t he d i s t a l 5 ' 3 ' ga l ago s e -


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262

HUM CHI GOR ORA HLA MAC A T E T A R G A L L E M R A B GOA

H U M AN 1 . 7 1 .8 3 . 3 4 .3 7 . 0 1 0 . 8 2 4 . 6 2 9 . 9 2 2 . 6 3 1 . 7 3 1 . 11 . 7 1 . 8 3 . 4 4 . 5 7 . 4 1 1 . 6 2 9 . 8 3 6 . 5 2 6 . 9 4 1 . 2 4 0 . 2

C H IM P 1 5 8 0 1 1 . 7 3 . 5 4 . 7 7 . 0 1 0 . 8 2 5 . 8 3 1 . 6 2 3 . 4 3 2 . 4 3 1 . 61 . 8 3 . 6 4 . 8 7 . 4 1 1 . 7 3 1 . 7 4 1 . 1 2 8 . 0 4 2 . 4 4 1 . 1

G O R I LL A 1 2 5 4 3 1 1 6 8 3 3 . 5 4 . 7 7 . 2 1 0 . 9 2 6 . 0 3 0 . 0 2 3 . 8 3 3 , 8 3 2 . 33 . 6 4 . 8 7 . 5 1 1 . 8 3 2 . 0 3 8 . 3 2 8 . 6 4 4 . 8 4 2 . 2

O R AN G 1 6 7 5 2 1 0 5 9 1 1 0 7 7 9 4 . 7 7 . 3 1 0 . 8 2 4 . 8 2 8 . 0 2 3 . 1 3 0 . 2 3 1 . 54 . 8 7 . 7 1 1 . 7 3 0 . 2 3 5 . 0 2 7 . 6 3 8 . 6 4 0 . 8

G IB B O N 7 5 2 3 7 1 1 9 7 5 1 3 7 2 1 2 7 . 5 9 .8 2 6 . 3 2 9 . 3 2 3 . 2 3 3 . 1 3 1 . 88 . 0 1 0 . 5 3 2 , 4 3 7 . 2 2 7 . 7 4 3 . 7 4 1 . 4

M A C A C A 1 6 4 5 3 1 5 6 3 9 1 1 7 6 9 1 1 1 6 0 7 1 8 2 1 1 . 9 2 6 . 0 3 1 . 4 2 4 . 3 3 2 . 4 3 3 . 31 3 . 0 3 2 . 0 4 0 . 8 2 9 . 3 4 2 . 4 4 3 . 9

AT E L ES 1 1 8 9 6 9 7 8 4 1 0 4 1 8 1 1 2 3 6 6 7 8 9 1 0 6 6 0 2 7 . 1 2 9 . 7 2 5 . 3 3 3 . 7 3 2 . 63 3 . 6 3 7 . 8 3 0 . 8 4 4 . 7 4 2 . 7

T A R S IE R 8 0 1 0 4 5 7 7 3 9 1 3 5 1 1 8 2 3 5 2 5 5 3 7 4 1 9 7 3 0 . 6 2 5 . 4 3 4 . 3 3 4 . 23 9 . 3 3 1 . 0 4 5 . 8 4 5 . 6

G A L AG O 6 1 9 7 3 7 5 3 3 5 5 8 3 3 8 7 2 1 0 3 3 8 9 2 2 2 2 1 5 3 4 1 2 1 . 9 3 6 . 2 3 6 . 42 6 . 9 4 9 . 5 4 9 . 7

L EM U R 5 0 3 3 2 3 5 1 2 2 1 7 3 4 6 6 1 2 2 9 2 5 3 4 2 1 9 6 4 6 5 7 3 9 3 3 3 0 . 1 2 9 . 43 8 . 4 3 7 . 4

R A B B I T 6 0 8 4 2 4 6 7 2 1 6 3 3 1 7 9 9 79 3 0 5 2 2 1 9 4 5 2 2 4 4 6 0 5 3 7 0 1 3 5 . 74 8 . 5

G O A T 3 7 4 7 2 4 1 9 2 2 6 6 3 1 4 3 16 5 0 2 4 2 1 1 8 6 6 3 44 4 3 0 6 5 2 5 6 8 1 8 3 7

Fig. 1 . I n t e rs p e c i e s d is t a n c e s a s e s t i m a t e d f r o m p a i r w is e c o m p a r i s o n s o f o r t h o lo g o u s n o n c o d i n g s e q u e n c e s f r o m ~ - t y p e g l o b in l o c ia n d t h e i r f la n k in g a n d i n t e r g e n i c D N A . T h e n u m b e r s a b o v e t h e d i a g o n a l a r e p e r c e n t s e q u e n c e d i ff e re n c e v a lu e s ( c a l cu l a te d a s t h en u m b e r o f s u b s t it u t io n s p l u s th e n u m b e r o f g a p s d iv i d e d b y t h e t o t a l n u m b e r o f s h a r e d n u c l e o t i d e p o s it i o n s p lu s t h e t o t a l n u m b e ro f g a ps , w i t h t h e p r o d u c t o f t h e d i v i s i o n m u l t i p l i e d b y 1 0 0) u n c o r r e c t e d f o r s u p e r i m p o s e d s u b s t i t u ti o n s ( to p n u m b e r s i n t h e s l o ts )a n d c o r r e c te d f o r s u p e r i m p o s e d s u b s t i tu t i o n s ( b o t t o m n u m b e r s i n t h e s lo t s) b y t h e m e t h o d o f J u k e s a n d C a n t o r ( 1 9 6 9 ). F o r e a c h s l o tt h e n u m b e r s b e l o w t h e d i a g o n a l a re t h e n u m b e r o f a l ig n e d n u c l e o t id e s e q u e n c e p o s i t i o n s i n t h e p a ir w i s e c o m p a r i s o n . B e c a u se t h e

d u p l i c a t e d T- g l o b i n g e n e s o f c a t a r r h i n e p r i m a t e s s h o w p a t c h y c o n v e r s i o n s i n i n t r o n 2 r e g i o n s ( S l i g h t o m e t at . 1 9 8 8 ) , w e d i d n o t i n c l u d e7 i n t r o n 2 s e q u e n c e s o n c o m p i l in g t h e o r t h o l o g o u s n o n c o d i n g s e q u e n c e s f o r t h e p r e s e n t s tu d y.

q u e n c e w i t h t h e o r t h o l o g o u s r a b b i t s e q u e n c e ( M a r -go t e t a l. 1989 ). We a l so add mo re 5 ' f lank ing -/s eque nce f rom go r i ll a and , i n a l l new r eg ions o f t hee x p a n d e d a l i g n m e n t , t h e m a t c h i n g h u m a n o r t h o -logue .

I n t e r s p e e i e s D N A D i s t a n c e s a n d B r a n c h i n gP a t t e rn i n P r i m a t e E v o l u t i o n

Figu re 1 p r e sen t s a ma t r i x o f pe rce n t s eque nce d i f -f e r en c e v a l u e s f o u n d i n p a i r w i s e c o m p a r i s o n s o f h u -man , ch impanzee , go r i l l a , o r angu tan , g ibbon , ma-caque , sp ide r mo nke y, t a r s i e r, ga lago , l emur, r abb i t ,a n d g o a t o r t h o l o g u e s . E a c h o r t h o l o g u e c o n s i s t s o fn o n c o d i n g n u c l e o t i d e s e q u e n c e s f r o m t h e g e n o m i creg ion con t a in ing t he f i - t ype genes o f t ha t spec i e s.A s p o i n t e d o u t i n G o o d m a n e t a l. (1 9 8 9 ), t h e c o d i n gsequ enc es of the f ive typ es of loc i (~, % ff~ , 5 , f i) in

t h is g e n o m i c r e g i o n o f a p r i m a t e a c c o u n t f o r le s st h a n 5 % o f t h e r e g io n a n d t h e n o n c o d i n g n o n r e g u -l a t o r y s e q u e n c e s a c c o u n t f o r a t le a s t 9 5 % o f t h er e gi o n . T h e m o s t e x t e n s i v e s t r e tc h o f c o n t i n u o u s

n o n c o d i n g n o n r e g u l a t o r y D N A f r o m t h i s g e n o m i cr e g io n , t h a t w e h a v e s e q u e n c e d i n e a c h o f t h e f i v eh o m i n o i d s a n d i n r h e s u s a n d s p i d e r m o n k e y s , is t h e10 .8-kb lo ng s t re tch tha t c rosse s the ~7-g lobin pseu -dogen e o r fro l ocus . I n t he ca se o f t he g ibbon ~koregion , i t i s s t i l l be ing sequenced (F i tch e t a l . , un-p u b l i s h e d ) b u t c o n s i s t s p r e s e n tl y o f a b o u t 6 .5 k b o fc o n f i r m e d s e q u e n c e . T h e b o t t o m o f F ig . 2 p r e s e n t st h e m a t r i x o f p e r c e n t s e q u e n c e d i f f er e n c e s f o r t h e s ee x t e n s i v e ~ o r t h o l o g u e s f ro m t h e s e v e n p r i m a t e s .F i g u r e 3 c o m p a r e s t h e p e r c e n t s e q u e n c e d i f f e r e n c ev a l u e s f ro m t h e s e o r t h o l o g o u s c o m p a r i s o n s o f s e -q u e n c e d n o n c o d i n g D N A s t o t h e in t er s pe c i es D N Ad i st a n c es r e p o r te d f r o m D N A h y b r i d iz a t i o n d a t a b yS i b l e y a n d A h l q u i s t ( 1 9 8 7 ) f o r c a ta r r h i n e s a n d b yB o n n e r e t a l . ( 1 9 8 0 ) f o r m o r e a n c i e n t l y s e p a r a t e dp r ima te l i neages .

In F ig. 3 , t he g loba l measu re s o f gen om ic s e -q u e n c e d i v e rg e n c e p r o v i d e d b y t h e d e l ta Ts o H v a l -

u e s o f t h e D N A h y b r i d i z a t i o n d a t a c o r r e l a t e c lo s e l yw i t h t h e p e r c e n t s e q u e n c e d i f f e r e n c e v a l u e s f r o mp a i r w i s e c o m p a r i s o n s o f t h e k n o w n o r t h o l o g o u sn o n c o d i n g n u c l e o t i d e s e q u e n c e s . T h e c o r r e l a ti o n f o r


4/7

t1 . 0 3

0 . 4 2

0.72

0 . 8 0 0 . 9 0

0 . 8 9

1 . 8 2

C

GI0

2 . 5 8 G b

4 . 6 5 R

8 . 3 5

263

H . . . . .

C 1.62 .. .. .

G 1.72 1.85 .. ..

O 3.44 3.55 3.55 .. .. .

Gb 4.46 4.92 4.65 4.90

R 7.74 7.89 7.74 7.79

S I 1.48 11.69 1 1.47 l 1.60

H C O 0

8.39 .....

11.83 13.00 .....

Gb R S

Fig. 2. Neighbor-joi ning tree for the data set of orthologousnoncoding sequences spanning the ~/-globin locus and extendingtoward the G ocus. This data set consisted of human (H), chim-panzee (C), gorilla (G), orangutan (O), gibbon (Gb), rhesus mon-

key (R), and spider monke y (S) orthologues. Below the tree is thedistance matrix used to calculate the neighbor-joining tree by thealgorithm of Saitou and Nei (1987). The dis tance matrix is shownas percent sequence difference values correcte d for superimpose dmutati ons by the metho d of Jukes and Cantor (1969). Branchlengths represent the number of changes per 100 base positionsincorpora ted along each lineage.

t he anc i en t l y s epa ra t ed p r ima te l i neages i s pe rhapse v e n m o r e a m a z i n g t h a n f o r t h e c a ta r r h in e s , i n th a to n e w o u l d e x p e c t t h e d e l t a Ts o H v a l u e s t o b e c o m ele ss accu ra t e a t t he se l a rge r phy log ene t i c d i s t ances .Inde ed on t h i s ba s i s , Sa r ich e t a l. (1989 ) d i s co un te dthe f i nd ing o f Bo nne r e t a l . ( 1980 ) t ha t t he l emu r i -f o r m b r a n c h o f p r i m a t e s e v o l v e s a t t h e D N A l e ve la t a m u c h s l o w e r r a t e t h a n e i t h e r t h e l o r i si f o r m o rt a r s i e r b r anches . Ye t , we s ee t he s am e pa t t e rn fo rt h e o r t h o l o g o u s n o n c o d i n g s e q u e n c e s f r o m E - t y p eg lob in l oc i and t he i r f l ank ing and i n t e rgen i c r eg ions(Koop e t a l . 1989 ) . I n f ac t i n t he t r ee t ha t summa-r i z e d t h e c o m b i n e d r e s u l t s f r o m a l l o r t h o l o g o u sn o n c o d i n g n u c l e o t i d e s e q u e n c e p o s i t i o n s a n d c a l -c u l a t e d b r a n c h l e n g th s b y t h e p r o c e d u r e o f F i t c h

a n d M a rg o l i a s h ( 1 9 67 ) , w e f o u n d t h e l e n g t h o f t h el e m u r b r a n c h t o b e o n l y o n e - h a l f t h e l e ng t h o f t h ega l ago b ran ch (F ig . 4 i n K oo p e t a l. 1989 ).

O u r s t r o n g es t e v i d e n c e f o r th e b r a n c h i n g p a t t e r no f m a j o r p r i m a t e c l ad e s c o m e s f r o m t h e m a x i m u mp a r s i m o n y t re e s c o n s t r u c t e d f o r t h e s e p a r a t e s e t s o fa l i gned nuc l eo t i de s equence o r tho logues , t he se s e t sreprese nt ing the e , % r /, 5 , an d f l loc i pro pe r an d theex t ended 10 .8 -kb i f0 r eg ion (Koop e t a l . 1989 ) . Asr e v i e w e d i n t h e i n t r o d u c t i o n t o t hi s p a p e r , t h e s et r ee s s u p p o r t t h e d i v i s i o n o f P r i m a t e s i n t o S t r e p -s ir h in i ( t h e l e m u r i f o r m - l o r i s i f o r m c l a d e) a n d H a p -l o r h i n i ( t h e t a r s i e r - A n t h r o p o i d e a c l a d e ) , a n d A n -t h r o p o i d e a i n t o P l a ty r r h i n i ( th e N e w Wo r l d m o n k e yc la d e) an d C a t a r rh i n i ( th e O l d Wo r l d m o n k e y - h o m -ino id c l ade ).

T h e e x t e n d e d ~ r e g i o n o r t h o l o g u e s p r o v i d e t h el a rg e st p o r t i o n o f t h e p a r s i m o n y e v i d e n c e o n t h ec l ad i s t ic r e l a t i onsh ips o f ho mi no id l ineages . F igu re4 s h o w s t h e m o s t p a r s i m o n i o u s t r e e f o u n d f o r t h i sd a t a s e t o f s p i d e r m o n k e y, r h e s u s m o n k e y , g i b b o n ,o r a n g u t a n , g o r i l l a , c h i m p a n z e e , a n d h u m a n o r t h o -l o g ue s . T h e n u m b e r o n t h e s t e m t o e a c h n o d e i s t h ed i f f e r ence i n t r ee l eng ths be tween the mos t pa r s i -m o n i o u s t r e e a n d t h e n o n p a r s i m o n i o u s t r e e t h a tadds t he l e a s t l eng th i n b r eak ing up t he c l ade r ep -r e s e nt e d b y th a t s t em . T h u s t h e h u m a n - c h i m p a n z e ec l ade i s supp or t ed by a d i f f e r ence va lue o f 8 , theh u m a n - c h i m p a n z e e - g o r i l l a c l a d e b y 5 4, t h e h u -m a n - - c h i m p a n z e e - g o r i l l a - o ra n g u t a n c l a d e b y 20 ,a n d t h e h u m a n - c h i m p a n z e e - g o r i l l a - o r a n g u t a n -

g i b b o n c la d e b y 4 0. T h e s u p p o r t f o r a h u m a n - c h i m -panze e c l a r e com es f rom th e fu l l 10 .8 -kb fi n r eg ion ;t h i s f o ll o w s f r o m t h e f a ct t h a t t h e n o n p a r s i m o n i o u st r ee s t h a t a d d e d t h e l e a st l e n g th a b o v e t h e m a x i m u mp a r s i m o n y l e n g th e i t h e r j o i n e d h u m a n a n d g o r i ll ao r t h o l o g u e s fi rs t o r j o i n e d c h i m p a n z e e a n d g o r il lao r tho logues f i r st ( e ach o r tho logu e be ing abo u t 10 .8k b l on g ). H o w e v e r, t h e s u p p o r t f o r t h e o t h e r c l a d e sd e p i c te d b y t h e s t e m s o f t h e m a x i m u m p a r s i m o n yt r ee c o m e s f ro m o n l y t h a t p o r t i o n o f t h e e x t e n d e df in reg ion ( a bou t t h r ee - f i f t h s o f i t) t ha t ha s so f a rb e e n s e q u e n c e d i n g i b b o n ; i n e a c h c a s e i n t h e n o n -

p a r s i m o n i o u s t r ee t h a t a d d e d t h e l e as t l e n g th t o t h em a x i m u m p a r s i m o n y l e n gt h, t h e g i b b o n b r a n c he i t h e r b r o k e u p t h e c l a d e i n q u e s t i o n o r w a s t h eb r a n c h t h a t l e f t t h e c l a d e t o j o i n a n o u t s i d e b r a n c h .


5/7

264

G L O B I N C L U S T E RN O N C O D I N G S E Q U E N C E% D I V E R G E N C E

H U M A N - C H I M P 1 . 7H U M A N G O R I L L A 1 .8H U M A N - O R A N G 3 . 3H U M A N - G I B B O N 4 . 3H U M A N - R H E S U S 7 . 0

H U M A N - AT E L E S 1 0 . 8C H I M P - G O R I L L A 1 . 7C H I M P - O R A N G 3 . 5C H I M P - G I B B O N 4 . 7C H I M P - R H E S U S 7 . 0G O R I L L A - O R A N G 3 . 5G O R I L L A - G I B B O N 4 . 7G O R I L L A - R H E S U S 7 . 2O R A N G - G I B B O N 4 . 7O R A N G - R H E S U S 7 . 3G I B B O N - R H E S U S 7 . 5H U M A N - TA R S I E R 2 4 . 6H U M A N - G A L A G O 2 8 . 9H U M A N - L E M U R 2 2 . 6AT E L E S - TA R S I E R 2 7 . 1AT E L E S - G A L A G O 2 9 . 7AT E L E S - L E M U R 2 5 . 3TA R S I E R - G A L A G O 3 0 . 6TA R S I E R - L E M U R 2 5 . 4G A L A G O - L E M U R 2 1 . 9

1 0 . 8 K BV~ S E Q U E N C E% D I V E R G E N C E

1.61.73 .44 .37. 4

10.61.83. 54. 87 .53. 54 .57 .44. 87 .47. 9

~From Sib ley and Ahlquls t (1987) J . M o L E v o L 2 6 : 9 9 - 1 2 1 .2 F r o m B o n n e t e t a l (1980) N a t u r e 286:420-423.

G E N O M I CD N A - D N A H Y B .ATsoH

1.612. 33 .64 .87.3 6,9 2

11.22. 23. 65.17 .33 .64 .57 .24 .97 .47.1

25.428.022.326.430.724.530.225.822.1

Fig. 3. Comparison of inter-species distances as estimatedfrom ortbologous noncodingsequences and as estimatedfrom cross hybridization of to-tal single-copy genomic DNAs.The distance values are notcorrected for superimposedsubstitutions. The percent di-vergence values for B-globincluster noncoding sequencesare taken from Fig. 1. In thecolumn labeled 10.8-kb ~n se-

quence, the gibbon is not rep-resented by the full 10.8 kb ofthis noncoding region but isrepresented by about 6.5 kb ofit (see text).

T a x o n o m i c C o n c l u s io n s

As noted in the introduction, traditional taxonomicclassifications are mixture s o f grades and clades withmodem revisions usually favoring the substitutionof clades for grades. The classification of hom ino idgenera used by Simpson (1945), and later revisedby him (Simpson 1963), serves as a starting pointfor the further revisions that we propos e to achievea strictly cladistic classification. We shall ignore thefossil hominoids as outside our data and field ofexpertise but do not see any insurmountable diffi-culties in eventually including them in a classifica-tion that reflects the cladistic hypotheses best sup-ported by the combined evidence from living andfossil forms. Simpson (1945) divided superfamily

Hominoidea into the Pongidae for all apes and theHominidae for humans; he subdivided Pongidaeinto two subfamilies: Hylobatinae containing Hy-lobates (co mmon gibbons) and Symphalangus (sia-mang gibbons) and Ponginae containing Pongo(orangutans), Pan (chimpanzees), and Gorilla (go-rillas). He followed this same scheme in his 1963work, except that he placed all extant gibbons inHylobates and, similarly, he placed the living Af-r ican apes (common chimpanzees , pygmy chim-panzees, and gorillas) in Pan. This showed that theliving African apes are more closely related to one

another than to orangutans and that the great apes(orangutans, chimpanzees, and goril las) are moreclosely related to one another than to the gibbonsor lesser apes. I f only human s could be ignored,

- - H

- - C

G

O

G b

R

S

Fig. 4. The maximum parsimony tree found for the seven ex-tended ~q region nucleotide sequence orthologues after exam-ining aU 945 of the possible unrooted trees that seven sequencescan form. The circled number on each stem to a branching nodeis the difference n tree lengths between the maximum parsimony

tree and the nonparsimonious tree that adds the least length inbreaking up the clade represented by that stem. For example, themaximum parsimony tree requires 2036 sequence changes (num-ber of nucleotide substitutions plus number of insertions anddeletions), and each nonparsimonious tree that adds the leastlength (gorilla grouping with either human first or chimpanzeefirst) requires 2044 sequence changes; thus the circled numberon the stem to the human-chimpanzee clade is 8.

Simpson's 1963 classification was strictly cladistic.Because humans could not be ignored, Simpsonplaced us in the family Hominidae; only this t ime

accepting the evidence that the extinct ape genusAustralopithecus was the direct ancestor of Homo,he removed Australopithecus f rom Pongidae andplaced it in Hominidae. Despite these cladistic re-


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f i n e m e n t s o f h i s 1 9 4 5 c l a s s i fi c a ti o n , h i s w i d e l y a c -c e p t e d 1 9 6 3 c l a ss i f ic a t io n o f h o m i n o i d g e n e r a s ti llh a s P o n g i d a e a s a g r a d e t a x o n i n t h a t n o t o n l y a r et h e g r e a t a p e s o f h i s P o n g i d a e m o r e c l o s e ly r e la t e dt o h u m a n s t h a n t o g i b b o n s , b u t a l so t h e A f r i c ang r e a t a p e s a re m u c h m o r e c l os e ly r e l a te d t o h u m a n st h a n t o o r a n g u t a n s a n d g i b b o n s . S i m p s o n h a d a c -

c e p t e d t h e p r o t e i n e v i d e n c e ( G o o d m a n 1 9 6 2, 1 9 6 3 ;Z u c k e r k a n d l 1 9 6 3) t h a t th e A f r i c a n a p e s sh a r e am o r e re c e nt c o m m o n a n c e s tr y w i th h u m a n s t h a nw i t h o r a n g u t a n s b u t r e j ec t e d th e p r o p o s a l t h a t t h eA f r ic a n a p e s b e l o n g w i t h h u m a n s i n H o m i n i d a er a th e r t h a n w i th o r a n g u t a n s in P o n g i d a e ( G o o d m a n1 9 6 2 , 1 9 6 3 ). H e r e a s o n e d t h a t e a c h o f t h e li n e a g e st o t h e l i v i n g a p e s h a v e b e e n c o n s e r v a t i v e l i n e a g e sb u t t h a t th e l in e a g e t o h u m a n s h a s d i v e r g e d m a r k -e d ly in m o r p h o l o g y a n d b e h a v i o r f r o m t h es e a p el i n e ag e s a n d h a s e n t e r e d a n e w a d a p t i v e z o n e , t h u so n a g r a d e b a s i s d e s e r v i n g a n e w f a m i l y.

A t t h e g e n e t ic l e v e l o f s e q u e n c e d p r o t e i n s a n ds e q u e n c e d D N A , w e fi nd th e h u m a n l in e a g e t o b ej u s t as c o n s e r v a t i v e o r e v e n m o r e c o n s e r v a t i v e t h a ne a c h o f t h e o t h e r h o m i n o i d l in e a g es . M o r e o v e r , w ek n o w t h a t a s in g le m u t a t i o n a l e v e n t , e v e n a s s m a l la s a p o i n t m u t a t i o n i f i t h a p p e n s t o o c c u r a t a f u n c -t i o n a ll y i m p o r t a n t s i te in t h e D N A s e q u e n c e , c a ns o m e t i m e s h a v e a v e r y l a rg e p h e n o t y p i c e f f ec t o ni ts b e a r e r . T h u s i t s e e m s t o u s t h a t t o u s e g r a d ec o n c e p t s i n t a x o n o m y i s u n r e li a b le . T h e s e c o n c e p t sr e fl e c t a li n g e r in g a n t h r o p o c e n t r i c v i e w o f n a t u r e

a n d c o n v e y s u b j e c ti v e j u d g m e n t s a s t o w h i c h f e a -t u re s o f m o r p h o l o g y a n d b e h a v i o r a re i m p o r t a n t .T h e u s e o f c l ad i st ic c o n c e p t s p r o v i d e s a m o r e o b -j e c t i v e b a s i s f o r c l a s s i f i c a t i o n .

We p r o p o s e t h e f o l l o w i n g c l a d i s t i c c l a s s i f i c a t i o no f e x t a n t h o m i n o i d g e n er a .

S u p e r f a m i l y H o m i n o i d e aF a m i l y H o m i n i d a e

S u b f a m i l y H y l o b a t i n a eH y l o b a t e s

S u b f am i l y H o m i n i n a e

T r i b e P o n g i n iP o n g o

T r ib e H o m i n i n iS u b t r i b e G o r i l l i n a

Gor i l l aS u b t ri b e H o m i n i n a

P a nH o m o

W e a r e a g r e ei n g h e r e w i t h S i m p s o n ( 1 9 45 , 1 9 6 3)t h a t th e d i ff e re n t a p e g e n e r a w i th i n H o m i n o i d e aw h e n v i e w e d i n th e l i gh t o f a ll m a m m a l i a n s y s t e m -

a ti c s s h o u l d b e g r o u p e d t o g e t h e r in t h e s a m e f a m i l y ,b u t b e c a u s e w e w a n t a s t r ic t l y c l a d i st i c c l a s s i fi c a t i o nt h e ru l es o f t a x o n o m i c n o m e n c l a t u r e r e q u i re t h a ta ll t h e se a p e g e n e r a b e p l a c e d i n th e f a m i l y H o m i n i -

265

d u e . B y u s in g t h e c a t e g o r i e s o f s u b f a m i l y, t r i b e , a n ds u b t r i b e w e c a n g r o u p t h e g e n e r a a c c o r d i n g t o t h e i rc l a d is t ic r e l a ti o n s h i p s a s i n f e r r e d f r o m t h e b r a n c h -i n g p a t t e r n s h o w n i n F i gs . 2 a n d 4 . T h e l e a s t s tr o n g l ys u p p o r t e d g r o u p i n g i s t h a t w h i c h p l a ce sP a n a n dH o m o t o g e t h e r t o t h e e x c l u s i o n o fGori l la . C l e a r l y,t h e d i v e r g e n c e e v i d e n c e f o r t h is i s w e a k . H o w e v e r ,

t h e p a r s i m o n y e v i d e n c e , in w h i c h o r t h o l o g o u s n o n -c o d i n g s e q u e n c e s s p e c if i ca l ly g r o u pP a n a n d H o m o ,a p p e a r s t o b e s t a ti s ti c a ll y s i g n i fi c a n t ( Wi l l i a m s a n dG o o d m a n 1 98 9) . We h a v e c h o s e n to g r o u p c h i m -p a n z e e s w i th h u m a n s i n s u b tr i b e H o m i n i n a r a t h e rt h a n i n g en u s H o m o f o r t w o r e a s o n s . F i r s tl y , t h ed i v e r g e n c e b e t w e e n t h e tw o c h i m p a n z e e s p e c i es , P.t rog lodytes ( c o m m o n c h i m p a n z e es ) a n dP. p a n i s c u s( p y g m y c h i m p a n z e e s ) , i s l es s t h a n t h e d i v e r g e n c eb e t w e e n c h i m p a n z e e s( P a n ) a n d h u m a n s ( H o m o ) .S e c o n d l y, o u r s c h e m e s ti ll a l l o w s p a l e o a n t h r o p o l -o g i s ts t o g r o u p a u s t r a l o p i t h e c i n e s p e c i e s c l o s e r t oH o m o s ap ie n st h a n t o a n y l i v i n g a p e s . T h i s c a n b ed o n e w i t h i n t h e g e n u sH o m o b y u s i n g t h e c a t e g o r i e so f s u b g e n u s a n d s p e c ie s .

Acknowledgments.This work was supported by NS F grant BSR8607202, NIH grant HL 33940, and a grant from the Center forMolecular Biology at W ayne State Un iversity.

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Primate Evolution at the DNA Level