4
PLATYRRHINES , CATARRHINES AND THE ANTHROPOID TRANSITION
Alfred. L. Rosenberger,
Dept. of A n t h r o p o l o g y ,
University of I l l i n o i s a t Chicago,
BOX
4348,
Chicago, I l l i n o i s 60680, USA.
Ih?L'RODUCTION
Four b a s i c questions a r e fundamental t o our i n q u i r i e s i n t o t h e
o r i g i n s and e a r l y h i s t o r y of t h e anthropoid primates: (1) A r e p l a t y r r h i n e s
and c a t a r r h i n e s monophyletically or d i p h y l e t i c a l l y r e l a t e d ? ( 2 ) How did
t h e i r g e o g r a p h i c a l d i v i s i o n i n t o N e w and Old World r a d i a t i o n s come about?
( 3 ) Who were the ancestors of t h e a n t h r o p o i d s ? ( 4 ) What adaptive breakthroughs, i f any, were achieved d u r i n g the a n t h r o p o i d t r a n s i t i o n ? These
l a r g e , much debated s u b j e c t s w i l l be t h e t o p i c of t h i s paper, scaled down
t o a s i z e and f o r m u l a t i o n t h a t w i l l perhaps suggest more questions than i t
answers. Another equally basic m a t t e r , predicated on the o t h e r s and t h e r e f o r e more i n t e r e s t i n g in many ways, i s : What are the d i f f e r e n c e s between
t h e p l a t y r r h i n e and catarrhine adaptive r a d i a t i o n s , and how can they be
explained? That t h i s m o r e comparative concern has r e c e i v e d a t t e n t i o n only
recently (Delson & Rosenberger, 1984) i s i n l a r g e p a r t due t o the i m balance of fossil evidence f o r the Old and New World a n t h r o p o i d s . Despite
i t s i n t e r e s t , it i s a question t h a t will n o t be c o n s i d e r e d i n t h i s paper.
Monophyl y or d i p h y l y - how a r e p l a t yrrhines and ca t a r r h i n e s
re1 at ed ?
The obvious d i s t i n c t i o n s between l i v i n g p l a t y r r h i n e s , c a t a r r h i n e s and other primates were w e l l known t o the a u t h o r s of the e a r l i e s t
higher Level p r i m a t e c l a s s i f i c a t i o n s (e.g. E. Geoffrey, 1 8 1 2 ; Gray, 1 8 2 1 ) .
More d e t a i l e d work on s k e l e t a l morphology (e.g. Mivart, 1874; Flower, 1866)
expanded t h e range of t h e i r d i f f e r e n c e s , and it was this b d y of evidence
t h a t formed t h e backdrop f o r t h e o r i e s of t h e a f f i n i t i e s of p l a t y r r h i n e s
and c a t a r r h i n e s . Two s c h o o l s of thought emerged. One s u g g e s t 4 t h a t a n t h r o p o i d s w e r e the monophyletic descendants of a s i n g l e protoanthropoid a n c e s t o r
that was g e n e a l o g i c a l l y l i n k e d with a non-anthropoid ( v a r i o u s l y s p e c i f i e d
a s adapid or ommyid). The other argued t h a t each group a r o s e i n p a r a l l e l
from distinct 'lower p r i m a t e ' s t o c k . Wood J o n e s (1929) a t t r i b u t e d the
o r i g i n s of the parallelism h y p o t h e s i s to S t . George Mivart (1874). who was
an a c c m p l i s h e d primate anatomist, but d e c i d e d l y apHylogenetic i n h i s
t h i n k i n g . Mivart seemed fascinated by cases of a d a p t i v e similarity i n
d i s p a r a t e taxonomic groups, such as the long armed A t e l e s and Hylobates,
the thumbless A t e l e s and Colobus and the long faced A l o u a t t a and Papio.
The o r i g i n s of t h e monophyly theory can probably be t r a c e d t o prjmatology's
p h y l a g e n e t i c a l l y o r i e n t a t e d thinkers, such a s E l l i o t Smith (19241, although
o t h e r prominent p h y l o g e n e t i c i s t s of t h e period, like Haeckel ( 1 8 9 9 ) and
Wood Jones (1929), w e r e convinced t h a t p l a t y r r h i n e s and c a t a r r h i n e s arose
independently. The complexity of the problem i s e v i d e n t when one r e a l i z e s
Rosenberger: The Anthropoid Transition
67
that Le Gros C l a r k , one of the m a s t e r s of comparative primate morpholqy,
opted for monophyly i n his f i r s t c l a s s i c synthesis of primate evolution
( 1 9 3 4 1 , but seemed swayed by d i p h y l y i n h i s heavily updated revision
(1363).
Although the m a j o r i t y of today's workers have r e j e c t e d t h e diphyly hypothesis, i t was t h e overwhelming favourite o f r e s e a r c h e r s u n t i l the l a s t
decade (e.g . Gregory, 1920; Schultz , 1969), and there i s l i n g e r i n g support
for it (e.g. Groves, 1972; Cachel, 1979, 1981). S i n c e this debate shaped
so much of modern p r h a t o l o g y , it would seem f i t t i n g to attempt a brief,
b u t by no means e x h a u s t i v e , historical synopsis and c r i t i q u e of t h e major
p r o p o s i t i o n s of the d i p h y l y theory ( F i g . 1).
L e t us examine t h r e e p r o p o s i t i o n s p e r t a i n i n g t o taxonmny, evolutionary
theory and g e q r a p h y , in sequence:
1. Platyrrhines and c a t a r r h i n e s a r e markedly different i n
form, s u g g e s t i n g a l a c k of a f f i n i t y and w a r r a n t i n g their separation a t
h i g h e r taxonomic l e v e l s ( e . g . Flower, 1866; Mivart, 1874; Keith, 1 9 3 4 ) .
2 . Primate h i g h e r t a x a should be ordered and interpreted as
s u c c e s s i v e grades of o r g a n i z a t i o n , r e f l e c t i n g t h e existence of d i r e c t e d
evolutionary trends, and s u g g e s t i n g t h a t advanced qrades of organization
could be attained, or traversed, independently by separate lineages ( e . q .
Huxley, 1863 ; Le G r o s C l a r k , 1963)
3 . The d i s j u n c t d i s t r i b u t i o n of New and Old World faunas were
p r d u c t s o f p a r a l l e l e v o l u t i o n , anthropoid primates being just one example
( e . g . Wallace, 1876; Matthew, 1915; Simpson, 1961).
.
A s M a r t i n (1973) e x p l a i n e d , using primate examples, classifications were
an i n s p i r a t i o n a l source fox evolutionary hypotheses, rather than the o t h e r
way around. A d d i t i o n a l l y , early classifications were usually devised as
aids t o z o o l o g i c a l i d e n t i f i c a t i o n , rather t h a n e v o l u t i o n a r y statements.
To m a i n t a i n such a typological structure and convey d i a g n o s t i c messages,
such c l a s s i f i c a t i o n s were exclusive i n design, that is, not b u i l t upon
t h e i n c l u s i v e n o t i o n s a k i n to the monophyly concept, or genealogy (Mayr,
1982) Consequently, when applied t o primates, the differences between
p l a t y r r h i n e s and catarrhines were exaggerated; when evolutionary questions
were posed, the answers were o f t e n c o r r e s p o n d i n g l y awry. Thus p l a t y r r h i n e s
and catarrhlnes w e r e assumed to be q e n e t i c a l l y f a r removed from one another
be genetically far removed from one a n o t h e r .
.
The g r a d i s t i c perspective, which implied an i n h e r e n t l y progressive orderi n g of groups n o t too d i f f e r e n t from the scala naturae p a r a d i g m which
preceded it ( e . 7 . Mayr, 1 9 8 2 ) , offered an e v o l u t i o n a r y explanation for
t h e set morphological dichotomies that distinguished taxa, The d i f f e r e n c e s
between platyrrhines and c a t a r r h i n e s became explicable i f each had
attained somewhat different l e v e l s of e v o l u t i o n a r y rank along t h e trajectory e x h i b i t e d by L i v i n g primates (Fig. 1 ) . The s i m i l a r i t i e s of p l a t y r r h i n e s and c a t a r r h i n e s w e r e also thus e x p l a i n e d , s i n c e t h e e v o l u t i o n a r y
trends t h a t guided p r i m a t e d i v e r s i f i c a t i o n o p e r a t e d i n p a r a l l e l i n all
g r o u p s , e n a b l i n g each to reach comparable higher g r a d e s of organization.
Rosenberger : The Anthropoid T r a n s i t i o n
Fig. 1. The gradistic view of anthropoid evolution as a
parallel t r a n s i t i o n . Based upon t h e o r d e r i n g of " t y p e s " along
a scale of p r q r e s s ( s e e i n s e r t ) in the human direction,
allegedly c m o n evolutionary trends in groups across the
order and geographical division of possible ancestral stocks
(Diphyly I), l a t e r replaced by a less definite ancestraldescendant scheme (Diphyly 11).
Diagram showing general trend
of evolutionary development
from tree-shrew t o Homo.
8
t
I
...
iii
,,..
,.
Ape
C
a
I
I
:::
::i
::i
,..
Hominoid
ii:
:::
1
1
I
I
--Madagascar
I
-
+
-
-
-
-
-
Notharetlnes
PROSIMIAN STOCK
(Adapid or Ornomyid)
T - - - - - - 1
Microchoerines
I
- I - - - - - - -
Rosenberger: The Anthropoid Transition
69
Grades, like t a x a , were t y p o l o g i c a l l y defined. The s u g g e s t i o n
t h a t higticr t a x a d i d , i n fact, arise i n p a r a l l e l wag but a simple e x t e n s i o n
of the a s c e p t e d principle of convergent a d a p t i v e evolution a t the genus
l e v e 1. As men t ~ o n e d ,Mivart (1874) promulgated this viewpoint, and i t was
emphatically endorsed even d u r i n g recent t i m e s (Le Gros C l a r k , 1963).
Suppart for the theory came £ r a n the discovery of the e x t i n c t s u b f o s s i l
~ n d r ~ o i d ssuch
,
a s Hadropithecus and Archaeolemur, embraced by many
researchers (e.g. Wood Jones, 1929; Le Gros Clark, 1963) a s a sound
example of how parallelism i n p r i m a t e evolutionary trends can produce
a n t h r o p o i d ( o r monkey-) grade taxa o u t of an a n c e s t r a l stock of a lower
grade. The i n t e r p r e t a t i o n of marmosets a s a n a t o m i c a l l y primitive I e . g .
B e a t t i e , 1927) also seemed t o suggest t h a t p l a t y r r h i n e s had b r i d g e d the
h i g h e r primate grade s e p a r a t e l y from t h e c a t a r r h i n e s , which were never
suspected of having such primitive t r a i t s a s d i g i t a l claws and minimally
convoluted brains
.
Given t h i s a l l e g e d l y f a c t u a l b a s i s , i t was logically i n f e r r e d t h a t anthropoids had i n d e p e n d e n t l y evolved their s i m i l a r i t i e s , i n s i t a , i n the New
and Old Worlds. It w a s f r e q u e n t l y surmised that much of Tertiary mammalian
evolution was s e t t l e d d u r i n g the Eocene, when many modern families first
appeared in n o r t h e r n continents. C o u p l d w i t h t h e p a r a l l e l i s m principle,
and armed a g a i n s t t h e notion of imaginary land b r i d g e s across the oceans
at middle l a t i t u d e s , zoogeographers l i k e Wallace (1876) were convinced t h a t
Eocene primates, rodents and others i n d e p e n d e n t l y evolved i n t o more
advanced descendants after migratinq into s o a t h e r n c o n t i n e n t i h a v i n g
s i m i l a r t r o p i c a l environments. Rather convincing p a l a e o n t o l o g i c a l evidence
f o r this view was s u p p l i e d by Leidy (1873), Wortman (1903-41, and Gregory
(1920) among o t h e r s . They began t o c h a r t out t h e p h y l q e n e t i c h i s t o r y of
the major p r i m a t e groups as a n east-west hemispheric d i v i d e , which prog r e s s e d over time v i a southward d i s p e r s a l . I n many of these studies, Nurth
American n o t h a r c t i n e s w e r e p r m o t e d as p l a t y r r h i n e ancestors, European
michxochoerines were cited as c a t a r r h i n e and t a r s i i d ancestors, and
European adapines were possible s t r e p s i r h i n e ancestors. Following W a l l a c e ' s
e x p l i c i t r a t i o n a l i z a t i o n , the family-level segregation of t h e s e a n c e s t r a l
s t o c k s was emphasized a s proof t h a t a n t h r o p o i d s evolved d i p h y l e t i c a l l y i n
p a r a l l e l , a l t h o u g h Simpson ( e . g . 1961) perpetuated the mixture of phylogeny
and taxonmy by d e f i n i n g t h i s c a s e of p a r a l l e l i s m a s an example of monoPhYlY
--
-
In r e t r o s p e c t , one can appreciate how t h e p a r a l l e l i s m hypothesis provided
an e l e g a n t expianation of platyrrhine-catarrhine s i m i l a r i t i e s before
Darwin's monophyly concept became firmly established, and while t h e
approach of character weighting, c l a d i s t i c analysis and phylogeny
reconstmction w a s not broadly understood. I t would a l s o have been s o l i d
proof of the t h e o r e t i c a l e v o l u t i o n a r y p a t t e r n s championed by t h e 'New
Synthesis'. L i k e o t h e r cases in the h i s t o r y of science, a r e t h i n k i n g of
t h e d i p h y l y theory was perhaps slow i n coming because t h e data were p r e s e n t e d as a paradox, t o be answered by an unusual s o l u t i o n .
Since t h a t t i m e , r e v i s i o n s i n s y s t e m a t i c c o n c e p t s and methods, improved
knowledge of t h e affinities of a l l the p r i m a t e s , and a v a s t l y improved
70
Rosenberger: The Anthropoid T r a n s it ion
f o s s i l record have contributed t o t h e rejection of the h y p o t h e s i s t h a t
platyrrhines and c a t a r r h i n e s have evolved t o a n t h r o p o i d status
i n d e p e n d e n t l y . The g e n e a l o g i c a l relationships of the e a r l y T e r t i a r y
primates are b e t t e r appreciated, but their d e t a i l does n o t resolve i n t o
a n y t h i n g resembling t h e schemes that were conducive t o the d i p h y l y t h e o r y
elaborated by Gregory and o t h e r s (see S z a l a y & Delson, 1979; Rosenberger
et
- al.,
- 1 9 8 5 ) . Geography, which w a s c l e a r l y a s t r o n g e r b a r r i e r to ideas
than t o animal migration, now weighs less i n phylogeny r e c o n s t r u c t i o n . A s
e x t r i n s i c evidence, i t i s nut amer,able to tests of homology and polarity,
and, a t least i n i t i a l l y , should be ignored.
The recovery of more early Oligocene catarrhines and platyrrhines h a s
tended t o b l u r t h e i r anatomical distinctions. C h a r a c t e r a n a l y s e s of shared
p l a t y r r h i n e - c a t a r r h i n e t r a i t s (e.g Szalay & Delson, 1979: Luckett, 1980;
Delson & Rosenberger, 1980; C a r t m i l l et d l . , 1981; Rosenberger e t al.,
1985) provide direct s u p p o r t for their monophyletic d e s c e n t (see b e l o w ) ,
d e s p i t e sane nagging anatomical d i f f e r e n c e s which require better evolutionary e x p l a n a t i o n s . The ' a r c t o p i t h e c i n e ' t h e o r y of marmoset evolution, which
.
views callitrichines as primitive, has slowly eroded. More convincing
analyses have supported t h e idea that t h e y are a lineage of relatively
apomorphic structure and behaviour ( e . g . Rosenberger, 1983). The rampant
parallelisms that so impressed earlier workers (e.g. toothcombs i n lemurs
and lorises, suspensory l o c m o t i o n in gibbons and spider monkeys; i n c i p i e n t
o r complete postorbl t a l closure i n anthropoids, t a r s i e r s and e x t i n c t
i n d r i o i d s ; t h e manual dexterity of capuchin monkeys and c e r c o p i t h e c i d s )
are now g e n e r a l l y recognized as examples of incidental convergence, a n d
not evidence of true affinity, or as t r u e homology ( e . g . i n lemuriforms)
.
How, t h e n , do xecent a d v o c a t e s f i n d support f o r the diphyly i n t e r p r e t a t i o n ?
Cachel (1981) q u e s t i o n s s t u d i e s dealing directly with t h e issues (see
Ciochon % Chiarelli, 1980) and w r o n g l y defines the p l a t y r r h i n e - c a t a r r h i n e
r i d d l e a s "...the question of monophyly or diphyly of t h e anthropoid
qrade" (Cachel, 1981:168). It is the applicability of the 'grade' concept,
in this particular case, or in g e n e r a l , w h i c h i s i n q u e s t i o n ; s i n c e Darwin's
clear s t a t e m e n t of the phylogeny concept, propinquity of descent h a s been
the
hypothesis e x p l a i n i n g similarities shared jointly by s p e c i e s .
Damirl, who was a ' p h y l o g e n e t i c i s t ' [as opposed t o H u x l e y , who was a
'gradist'), wrote, i n his & s c e n t of Ma!:
Every n a t u r a l i s t , who believes i n the principle of
evolution w i l l grant that the two main d i v i s i o n s of
t h e Simiadae, namely the C a t a r r h i n e and P l a t y r r h i n e
monkeys, with t h e i r subgroups, have a l l proceeded from
one extreneljr ancient progenitor, before they had
diverged t o any c o n s i d e r a b l e e x t e n t from each other ...
The many characters which they possess in common can
h a r d l y have been i n d e p e n d e n t l y a c q u i r e d by s o many
distinct s p e c i e s . .." ( 1 8 7 1 p. 197-8).
To r e f u t e Darwin, one would have t o successfully c h a l l e n g e t h e assumption
t h a t such s i m i l a r i t i e s , especially i f d e r i v e d , are nonhcmologous. with the
s i n g l e exception of the p o s t o r b i t a l septum ( s e e below), there a r e no
Rosenberqer : The A n t h r o p o i d ~ r a n stion
i
71
p o t e n t i a l anthropoid synapomorphies w h o s e homology has been seriously
q u e s t i o n 4 on t h e basis of anatomy. N o r does functional r a t i o n a l i z a t i o n
detract from the phyletic valence of p o t e n t i a l synapomorphies simply
because we can better e n v i s i o n w h y samething evolved, which seems t o be
the premise of s o m e arguments ( C a c h e l , 1 9 7 9 ) . Rather, i t makes p u r e
similarity stronqer e v i d e n c e of affinity, because i t i m p l i e s the
inextricability of phylogeny a n r l a d a p t a t i o n .
There i s another aspect that d i s t i n g u i s h e s t h e s e alternative v i e w s of
p l a t y r r h i n e - c a t a r r l l i n e r e l a t i o n s h i p s . Only one i s s u b j e c t t o robust biol o g i c a l tests. The monophyly hypothesis is a relatively straightforward
c l a d i s t i c proposition. I t may be wrong, b u t i t l a y s o u t a set of facts
that have p
r e d i c t i v e v a l u e . I t can be c o r r o b o r a t e d by a b s o h i n g new data,
explaining a d d i t i o n a l anthropoid synapomorphies. I t i s not weakened by
zoogeographic uncertainties surrounding mechanisms t h a t drive groups to
d i s j u n c t i o n . Nor i s debate over the potential s i s t e r - g r o u p s of t h e anthropoids of relevance. P a r e n t h e t i c a l l y , its credibility i s increased now t h a t
the n o t h a r c t i n e - p l a t y r r h i n e / m i c h r o c h o e r i n e - c a t h i n e scenario has been
thoroughly discredited, without any a l t e r n a t i v e candidates being proposed
a s t h e twin, separate ancestors t o t h e p l a t y r r h i n e s and c a t a r r h i n e s .
other hand, the d i p h y l y hypothesis i s a more complex phylagenetic
and a d a p t a t i o n a l argument. It rests e n t i r e l y on the differences between
p l a t y r r h i n e s and c a t a r r h i n e s , relegating t h e i r s i m i l a r i t i e s t o trivia.
A s an ancestral-descendant. h y p o t h e s i s with no c l e a r statement of t h e
i d e n t i t y of its d u a l antecedents, i t i s a p h y l q e n e t i c hypothesis w i t h o u t
r o o t s in t h e world of experience. I f framed a s a cladistic hypothesis i n
which p l a t y r r h i n e s and c a t a r r h i n e s each have their own nonanthropoid s i s t e r
t a x a , i t w o u l d be menable t o t e s t , but I know of n o such p r o p o s i t i o n .
I f framed i n p u r e l y gradistic terms, i.e. a n t h r o p o i d s are descendants of
a s i n g l e non-strepsirhine, non-tarsiifom species t h a t had not yet evolved
t r a i t s such a s t h e f u s e d mandibular symphysis, p o s t o r b i t a l p l a t e or
c e l l u l a r petrosal b u l l a , it would s t i l l n o t be t e s t a b l e so long a s t h e
classic tests of homology, analogy and p o l a r i t y d e t e r m i n a t i o n a r e deemed
unacceptable (e.g. Cachel, 1981). The only recourse, given a d i s b e l i e f i n
t h e v a l i d i t y of classic tests, would be t o locate an a c t u a l c m o n
a n c e s t r a l s p e c i e s and examine its morphology, a v i r t u a l i m p o s s i b i l i t y .
On t h e
Zoogeography of earl g an throwids
Hoffstetter (1980) r e k i n d l e d an old debate when he proposed
t h a t t h e Oligocene catarxhines f r m the F a y u m su2ported t h e h y p o t h e s i s
t h a t a t r a n s a t l a n t i c migration of O l d World anthropoids gave rise t o
p l a t y r r h i n e s . Such c r o s s i n g s over l a n d bridges stretching between widely
s e p a r a t e d c o n t i n e n t s were f a v o u r i t e images among 'philosophical' zoologists of t h e n i n e t e e n t h c e n t u r y . ~t was r e j e c t e d by more modernistic
d i p h y l y and monophyly advocates ( e . g . Wallace, 1876; Matthew, 1915; Elliot
Smith, 19241, a l l of whom preferred a d i s p e r s i o n of anthropoids v i a the
n o r t h e r n continents. Hoffstetter, on the other hand, presented his case in
a d i r e c t , comprehensive fashion, based upon t h e premises that: (1) anthropoid monophyly i m p l i e d a camon origin i n the southern c o n t i n e n t s w h e r e
they a r e h a s i c a l l y endemic; ( 2 ) Egyptian p a r a p i t h e c i d s d i s p l a y e d m o r p h o l q y
consistent w i t h a k j p o t h e t i c a l p l a t y r r h i n e ancestor; ( 3 ) A f r i c a and S o u t h
72
Rosenberger: The Anthropoid Transition
America were c l o s e r together during t h e middle and l a t e Eocene, when
p l a t y r r h i n e s and catarrhines probably emerged and ( 4 ) t h e same explanation i s a p p l i c a b l e t o a second c o n t e n t i o u s group t h a t may have migrated
i n t o South h m e r i c a ' s i m u l t a n e o u s l y , the caviomoph rodents, thought by
Hoffstetter and c o l l e a g u e s (Lavocat, 1980) t o be t h e sister-group of t h e
African p h i a n y i d rodents.
Sane of t h e weaknesses of t h i s h y p o t h e s i s have been outlined ( e . g . Kay,
1980; Delson & Rosenberger, 1980) b u t l e t me c i t e several examples. Parap i t h e c i d s are an u n l i k e l y a n c e s t r a l s t o c k f o r t h e p l a t y r r h i n e s because,
as t h e i r anatomy becanes b e t t e r known, so t o o grows t h e l i s t of autapornorphous s p e c i a l i z a t i o n s (e.g. Szalay & D e l s o n , 1979; Kay & Sirnons, 1983)
that mark them a s a divergent c o l l a t e r a l c a t a r r h i n e branch. P o s t u l a t i n g a
d i f f e r e n t c a t a r r h i n e group as a p o s s i b l e p l a t y r r h i n e s i s t e r - t a x o n , such as
t h e p l i o p i t h e c i d s ( e . g . F l e a g l e & Bow.?, 19831, i s q u e s t i o n a b l e on similar
grounds. T h e i r g e n e r a l dental anatomy, which s e r v e s t o u n i t e c a t a r r h i n e s
as monophyletic ( e . g . Kay, 19771, is more derived t h a n t h e p l a t y r r h i n e
p a t t e r n . The l a t t e r probably lacked such c a t a r r h i n e traits as s t r o n g l y
d i f f e r e n t i a t e d t a l o n i d cusps, hypoconulids on f i r s t and second molars,
a u x i l i a r y wear facets on t h e back of t h e t r i g o n i d , subequal t r i g o n i d talonid e l e v a t i o n and advanced reduction of upper molar metaconules. Some
of these f e a t u r e s even suggest an e x t r a - A f r i c a n origin for c a t a r r h i n e s ,
which n e g a t e s t h a t crux of t h e t r a n s a t l a n t i c argument, the A f r i c a n endernism
of the c a t a r r h i n e s . The Burmese Pondaunqia displays than, possibly because
of a common ancestry shared w i t h catarrhines after t h e platyrrhinec a t a r r h i n e s p l i t (Delson a Rosenberger, 1980).
Regarding t h e former p o s i t i o n s of t h e continents, a f a c t o r t h a t s h o u l d be
treated separately f r a n the biological d a t a , b o t h t r a n s a t l a n t i c and t r a n s carribean c r o s s i n g s seem t o s t r e t c h t h e human imagination. W e r w a t e r
d i s t a n c e d u r i n g the Palaeogene would probably have been less of an impediment to primate dispersal than a c c e s s i b i l i t y t o island s t e p p i n g - s t o n e s ,
now t h a t sunken and/or r e s u t u r e d landmasses are thought t o have been
s c a t t e r e d between South America, and both North America and A f r i c a ( e . g .
Sykes et al., 1982; T a r l i n g , 19801, i n i n t e r r u p t e d chains. Finally, the
cladistic links between t h e African a n d South American r o d e n t s have been
seriously challenged i n a recent symposium on rodent phylogeny ( L u c k e t t &
Hartenberger, 1985).
The timing of the a r r i v a l of primates i n South America, and t h e a l l e g e d l y
equivalent emergence of related t a x a and S i m i l a r morphoLogies i n A f r i c a ,
is now a l s o being reconsidered. A r e v i s e d callibration of upper F a w
beds p l a c e s them e a r l i e r i n time, circa 32 m i l l i o n years ago, (Bohn &
Simons, 1 9 8 4 ) . N e w dates f o r the Branisella zone a t L a S a l l a , B o l i v i a , are
about 2 5 Mya (MacFadden, pers . c m . , roughly ten m i l l i o n y e a r s younger
than previously thought (Marshall et dl., 1 9 7 7 ) . By canparison w i t h the
anthropoid morphotype, t h e r e f o r e , t h e earliest known catarrhines were
h i g h l y modified d e n t a l l y perhaps t e n m i l l i o n y e a r s before t h e earliest
kqown p l a t y r r h i n e s , which t h e m s e l v e s are more primitive i n some ways
(Rosenberger 1901a, b ) but more d e r i v e d i n o t h e r s .
No
r e s o l u t i o n t o t21e p a l a e o z o q e q r a p h y question i s l i k e l y t o come without
Rosenberyer: The Anthropoid
rans sit ion
the recovery of f o s s i l s f r o m more African and South American localities,
which presently represent n o t h i n g more than two oases in an otherwise
desert of palaeontological ignorance. W e might profit, however, by placing
the question in a broader context. I t appears t h a t c o n t i n e n t a l Africa and
South America interacted with E u r a s i a and North America, respectively,
throughout the Tertiary, g i v i n g passage to d i f f e r e n t mammals at v a r i o u s
times. The Fayum contained a c i r c u i Tethyean fauna during the e a r l y Tertiary Ie.g. Cooke, 1972; Savage & Russell, 19831, s h a r i n g many elements
with s o u t h e r n Europe, the Indo-Pakistan region and c e n t r a l n o r t h A s i a
{Fig. 2 ) . I d e n t i c a l g e n e r a , families and ( p r o b a b l y ) s i s t e r - t a x a are present
o u t s i d e Africa and as far westward as N o r t h America, ranging in time from
late Palaeocene t o Oligocene (Table 1 1 . T h i s implies t h a t t h e F a p
accumulated (and probably supplied) a r a t h e r cosmopolitan mammalian fauna,
with the f l u x of the Tethys. The Fayum primates may have had an i m p o r t a n t
Fig. 2. A r e c o n s t r u c t i o n of the world's c o n t i n e n t s d u r i n g the
l a t e Eocene, made by Savage & Russell (1983). Several. orders,
families and genera of mammals (Table 1) were d i s t r i b u t e d across
t h e n o r t h e r n continents and into Africa. Protoanthropoids could
have been part of t h i s fauna but were e v e n t u a l l y d i v i d e d , as
when platyrrhines became isolated in S o u t h A m e r i c a . Eocene and
Oligocene primate localities a r e emphasized.
b
The World 4 1 Million Years Ago
America
Asia
America
Africa
Primate bearing localities
Land v e r t e b r a t e localitisa
Rosenberger: The Anthropoid T r c l n s i t i o n
74
geographic linkage with Asian forms (not having close relatives i n t h e
Eocene-Oligocene P a r i s Basin) and may be represented by a d i v e r s e assembl a g e of t a x a because they were a f f e c t e d en masse b y palaeogeography. The
p a r a p i t h e c i d s and e u c a t a r r h i n e s may
- have close t i e s w i t h forms akin t o
Pondaungia, as a l r e a d y mentioned. O l i g o p i t h e c u s , which does n o t appear to
h a v e any c a t a r r h i n e o r a n t h r o p o i d s y n a p m o r p h i e s , (less even than
Pondaungia possibly has) deserves more s e r i o u s comparisons with Indian
Indraloris (Szalay & Delson, 13741, w i t h t h e Chinese Hoangonius and w i t h
T a r s i u s . There i s a l s o l i t t l e doubt t h a t t h e African mcestors of the
Malagasy strepsirhines w i l l sane day t u r n u p , a s Africa probably supported
them en r o u t e t o Madagascar. These points t e n d t o argue against a n A f r i c a
t o South America dispersal route in pleading the a n t h r o p o i d s as a s p e c i a l
case, f o r they would be t h e o n l y group suspected of bridging the A t l a n t i c
and s u r v i v i n g the t r i p , and they would be t h e o n l y ones t o head westward.
I n t h e western hemisphere, a s i m i l a r p a t t e r n p r e v a i l e d , w i t h important
p h y l e t i c and geographic connections between N o r t h A m e r i c a and S o u t h ~ m e r i c a
(see McKenna, 1980) The d i d e l p h i d Alphadon w a s p r e s e n t i n t h e l a t e
Cretaceous of both c o n t i n e n t s , when t h e water barrier between them w a s
even greater than i n the Eocene. The contemporaneous c o n d y l a r t h , Perutherium,
resembles o t h e r s from t h e PaLaeocene and Eocene of North America, E u r o p e
and Asia. The exclusively North A m e r i c a n soricmorph insectivores also
seem t o have c o n t r i b u t e d t o t h e Neotro?ical realm during t h e Palaeogene,
leaving Solenodon and Nesophontes as d e s c e n d a n t s that a r e now confined to
the Greater Antilles (MacFadden, 1980). Thus, a smaller number of taxa
are t h o u g h t to have been involved i n an i n t e r c h a n g e between t h e Americas
than between A f r i c a and E u r a s i a , but this may reflect a more d i f f i c u l t
p a s s a g e across t h e geophysically complex p r o t o - C a r r i b e a n Basin. Primates
and rodents may simply represent one or t w o other cases of i n c i d e n t a l
dispersa 1.
.
Ancestors of t h e anthropoids
The t h r e e v i a b l e theories s p e c i f y i n g the sister-group, o r
a n c e s t r a l s t o c k , from which anthropoids a r o s e are respectively the adapida n t h r o p o i d , t a r s i i d - a n t h r o p o i d and omanyid-anthropoid hypotheses ( F i g . 3 ) .
T h e adapid-anthropoid h y p o t h e s i s i s based on a v a r i e t y of d e n t a l characteristics shared j o i n t l y by c e r t a i n fossils a n d all a n t h r o g o i d s , and the
case f o r i t h a s been made m o s t eloquently by Gingerich ( e . g . 1975, 1977,
1980). Previous f o r m u l a t i o n s of t h i s position ( e . g . Gregory, 1920; Le
Gros Clark, 1963) were f a l l a c i o u s l y i n f l u e n c e d by the scala n a t u r a e doctrine, an (apparent or u n c e r t a i n ) acceptance of a d i p h y l e t i c Anthropoidea,
a m i s u n d e r s t a n d i n g of the affinities of Palaeogene primates, and the
a c c i d e n t a l n a t u r e Of palaeontological discovery (Rosenberger e t a l . , 1 9 8 5 ) .
Sane of t h e c r a n i a l evidence s u p p o r t i n g the adapid-anthropoid hypothesis
has been c h a l l e n g e d r e c e n t l y (e.9. Rosenberger
S z a l a y , 1980; Delson 5.
R o s e n b e r g e r , 1980; Cartmill et al., 1981).
--
I n the d e n t i t i o n , t h e essential phenetic resemblance l i n k i n g adapids and
anthropoids includes such f e a t u r e s as a fused mandibular symphysis, spatul a t e incisors, canine sexual dimorphism, canine honing premolars and
upper molar morphology (e.g . G i n g e r i c h , 1980) . These have been reexamined
c r i t i c a l l y ( R o s e n b e r g e r e t a l . , 1985) and seriously challenged as a s u i t e
Rosenberger: The Anthropoid T r a n s i tion
75
Table 1. Comparison of t h e geographical distribution of Fayurn
rnarmals d u r i n g the Eocene and Oligocene (cmpiled fran various
sources). The co-occurrence of genera in Europe, A s i a , North
America and Africa suggests t h e existence of a cosmopolitan
Laurasian fauna, and s i g n i f i c a n t interchange between A f r i c a
and Eurasia. The contrastingly sparse overlap between Fayum
groups and South American e u t h e r i a n s , and t h e i r restriction
t o the o r d i n a l l e v e l , suggests that Transatlantic crossings
a r e inconsistent with t h e global zoqeographic pattern for
n o n v o l a n t , terrestrial mammals. The presence of non-anthropoid
primates in the F a p m , such a s Oligopithecus, and t h e
possibility that Eocene forms like Pondaungia of Burma are
phyletically a n t h r o p o i d s - and more primitive than c a t a r r h i n e s
i m p l i e s that c a t a r r h i n e s may n o t be endemic t o A f r i c a and that
anthropoids arose on some other c o n t i n e n t .
Europe
PROMEUTHERIA
INSECTIVORA
MACROSCELIDEA
CH IROPTERA
Phyllostomatidae
PRIMATES
Parapithecidae
Quatrania
EropLiopithecus
Aeqyptopithecus
Family i n d e t .
Oligopithecus
RODENTIA
CREODONTA
Hyaenodontidae
Apterodon
Ptercdon
I sohyaenodon
PROBOSCIDEA
Moeritheriidae
SIRrnIA
EMBRITHOPODA
HYRACOIDEA
RHTIODACTYLA
Cebochoeridae
Rhagatherium
Brachyodus
MARSUPI ALI A
Didelphidae
I
Asia
8
•
North
America
south
America
Rosenberger: The Anthropoid Transition
of potential synapmorphies. Rosenberger et al. (1985) attempted to show
t h a t the anterior dentitions of those adapids most similar t o anthropoids
manifest a non-hmologous similarity, and are less comparable anatomically
than our vague t e r m i r ~ o l o q yallows. They i n t e r p r e t d t h e a n t e r i o r d e n t i tions of each group a s r e f l e c t i n g d i v e r g e n t adaptive o r i e n t a t i o n s , They
claim, for example, t h a t n o t h a r c t i n e s d i s p l a y a pattern laid over a bauplan
t h a t i s strepsirhine and not anthropoid. The p a t t e r n exhibits a reduction
in the importance of t h e anterior d e n t i t i o n i n ancestral adapids, away
from the p r i m i t i v e primate pattern where they play s i g n i f i c a n t harvesting
roles, towards a m o r e lemurifom-like s n i f f i n g and grooming complex
(Rosenberger & S t r a s s e r , 1985). This p o s t u l a t e d preadaptation t o a t o o t h combed anatmy rules o u t a p h y l e t i c adapid from anthropoid ancestry.
Adapids are thus viewed as bona fide representatives of t h e autapomorphous
s t r e p s i r h i n e clade. I n contrast, anthropoids augment the plesiadapiformlike p a t t e r n (see below), where food h a r v e s t i n g p r e d o m i n a t e s over the
g r o m i n g o r c o m u n i c a t i v e faculties associated with t h e anterior d e n t i t i o n
and s n o u t .
he t a r s i i d - a n t h r o p o i d hypothesis i s based upon a number of cranial
s i m i l a r i t i e s thought t o be exclusively shared by Tarsius and the anthrop o i d s , to the exclusion of a n m y i d s (Cartmill & Kay, 1978; C a r t m i l l , 1980;
C a r t m i l l et al., 1981). These characters include details of the middle ear
and t h e postorbital septum. S m e suggested synapomorphies, such as t h e
p a r t i t i o n i n g of an anterior bullar c a v i t y and t h e relocation of the posterior c a r o t i d foramen, have been challensed a s convergences (Rosenberger
& S z a l a y , 1980; Packer & Sarmiento, 1981). The homologizing of an enlarged
postorbital bar i n Tarsius and a complete postorbital s e p t u m i n anthropoids (see below) has also been disputed (Delson & Rosenberger, 1980).
Added t o these c r i t i c i s m s i s the f a c t o r of phylogeny. Although the p o s i t i o n
F i g . 3 . Anthropoid monophyly, and t h e three current candidates
f o r their a n c e s t r a l stock. Cknomyids (11) appear t o be t h e most
likely stem group.
MONOPHYLY
Platyrrhines
Catarrhines
Platyrrhines
Platyrrhines
Catarrhines
Catarrhines
Rosenberger: The Anthropoid Transition
77
of t a r s i e r s among t h e haplorhines i s i n d i s p u t e , advocates of t h e t a r s i i d anthropoid hypothesis bear t h e burden of f a l s i f y i n g a s e r i e s of possible
synapomorphies i n the skulls, d e n t i t i o n s and postcrania of T a r s t u s and the
microchoerines ( e . g . , Simons, 1 9 7 2 ; Gingerich, 1981; Rosenberger, i n prep.)
which would preclude them from s h a r i n g i n a s i s t e r - g r o u p relationship
with anthropoids.
The t h i r d o p t i o n , t h e anomyid-anthropoid h y p o t h e s i s , i s based upon features
d e m o n s t r a t i n g t h e rnonophyly of living h a p l o r h i n e s (Luckett k Szalay, 1978)
and the presence i n a n a n y i d s of a p p a r e n t l y derived h m o l o g i e s shared w i t h
anthropoids (Rosenbcrger % S z a l a y , 1980) such as an a p i c a l i n t e r o r b i t a l
septum, a b b r e v i a t e d face, e n l a r g e d b r a i n and, p o s s i b l y , f u s e d f r o n t a l
bones ( F l e a g l e & Rosenberger, 1983) . Those who object t o t h i s v i e w p o i n t ,
c i t i n g t h e presence of a fused t i b i o f i b u l a and t a r s a l e l o n g a t i o n ( e . g .
G i n g e r i c h , 19801, have been answered by t h e discovery of ommyid material
showing n e i t h e r of these d e r i v e d , non-anthropuid c o n d i t i o n s (Daqosto,
1985). This model i s also supported by its a b i l i t y t o provide a p r e a d a p t i v e
morphological substrate for the evolution of the a n t h r o p o i d head.
The anthropoid transition
The l i s t of shared derived f e a t u r e s which characterize t h e
Anthropoidea i s drawn from d i v e r s e anatomical systems, ranging from t h e
brain to the r e p r o d u c t i v e tract and t h e femur ( e . g . F a l k , 1980; L u c k e t t ,
1980; Ford, 1980). B u t as C a r t m i l l (1982) pointed out, these still g i v e
u s l i t t . l e i n s i g h t i n t o t h e l i f e s t y l e of early anthropoids, or t h e nature
of the a n t h r o p o i d t r a n s i t i o n . Gn t h e other hand, t h e c r a n i a l skeleton
includes the h i g h e s t concentration of anthropoid synapomorphies, which
suggests that a study of the a n t h r o p o i d head might shed more l i g h t on the
subject. Several of these synapomorphies, such as t h e fused mandibular
s y m p h y s i s , the p o s t o r b i t a l septum and t h e l a r g e , s p a t u l a t e i n c i s o r s have
been discussed as s i g n i f i c a n t contributions t o a m a s t i c a t o r y a p p a r a t u s
adapted t o a f r u g i v o r o u s diet ( e . g . Beecher, 1979; C a c h e l , 1979, Rosenberger e t a l . 1 9 8 5 ) . I am i n essential agreement w i t h this view, for
r e a s o n s other than t h o s e g i v e n b y Beecher, Cachel and others. L e t m e
propose a m o d e l for t h e e v o l u t i o n of the a n t h r o p o i d synapomorphies a s
a d a p t a t i o n s t o c r i t i c a l functions ( s e e Rosenberger & K i n z e y , 1976) f o r
the h a r v e s t i n g o f tough-coated fruits and, p o s s i b l y , f r u i t s w i t h hard
e d i b l e contents, such as seeds and nuts. The model i s framed a s a c o n t r a s t
of strepsirhine and anthropoid structure and f u n c t i o n and u s e s forms l i k e
Lemur and N o t h a r c t u s a s representatives of t h e primitive euprirnate anatomy
(Fig. 4 ) .
Anthropoid skulls are distinguished by features of t h e d e n t i t i o n , mandible,
facial structure, c r a n i o f a c i a l hafting and s t r u c t u r e of t h e ossified
petrosal b u l l a . I propose t h a t t h e transition t o the Anthropoidea involved
t h e e v o l u t i o n of a masticatory a p p a r a t u s designed to produce a powerful
a n t e r i o r bite employing the incisors and t h e anterior p r e m o l a r s effecting
s t r o n g static stresses w i t h i n t h e cranium. F u r t h e r , the a n a t m i c a 1 substrate f o r t h i s cmplex was a h a p l o r h i n e heritage; the particular mechanical solutions were c o n d i t i o n & by other architectural developments t h a t
emerged i n the m m y i d r e l a t i v e s of the a n t h r o p o i d s i n response t o d i f f e r e n t s e l e c t i v e pressures.
Rosenberger: The Anthropoid Transltlon
F i g . 4. Comparison of ( t o p ) anthropoid (Cebus) and ( b o t t o m )
euprimate (Lemur) skulls and dentitions to suggest some of
the m d i f i c a t i o n s involved in the a n t h r o p o i d t r a n s i t i o n :
(a)fused frontal bones, (b)recession of face, closure of o r b i t
by e n l a r g e m e n t and fusion of z y g m a t i c bone to braincase.
(clenhanced grinding stroke of chewing cycle, ( d ) cancellous
petrosal bones, (el fused mandibular symphysis , ( f ) fr o n t a t i o n
and e n l a r g e m e n t of i n c i s o r s , b l u n t i n g of premolars,
ANTHROPOID
Rosenberger: The Anthropoid Transition
The mst d i s t i n c t i v e component o f the anthropoid dentition i s
t h e morphology of the incisors. Anthropoid upper i n c i s o r s are quite
d i f f e r e n t from those of adapids (Rosenberger e
-.
t al.
- 1985), w i t h which they
have been compared. They are r e l a t i v e l y robust, high-crowned, buccol i n g u a l l y thickened t e e t h w i t h s t r o n g roots, and are aligned mostly in t h e
f r o n t a l p l a n e ( F i g . 4 ) They reciprocate w i t h lowers that are solidly
.
implanted across a f u s e d m a n d i b u l a r symphysis. Anthropoid upper premolars
tend to be m o r e transversely extensive and anteroposteriorly compact than
i s the case among other p r i m a t e s . They also have subsequal protocones and
paracones rather than a dominating buccal cusp, and there i s a f a i r l y
large intervening occlusal b a s i n . Molars tend t o have laraer occlusal
basins and have crowns of lower r e l i e f than those of many a n m y i d s , suggesting a t r a n s i t i o n a t sane point t o a g r e a t e r emphasis upon li-ngual phase
processinq during the chewing cycle (Kay & Hiiemae, 1974) Thus, i n general,
the molar teeth of anthropoids are designed for more crushing and grinding
and less shearing, and t h e premolars for more crushing than puncturing
d u r i n g the preparatory cycle.
.
t h a t the anthropoid head
r e f l e c t s a shift i n design f r m , a p r i m i t i v e euprimate p a t t e r n , i n which
the tooth-bearing f a c i a l skull i s braced a g a i n s t t h e cerebral s k u l l by an
envelope of midline s t r u c t u r e s , t o an architecture in which central and
lateral t r u s s e s are more prominent (Fig. 51, Geometrically, this corresponds
t o a repositioning of the face from a precerebral to a more subcerebral
location so that the face is hafted below the forebrain, rather than in
front of it. The primitive euprimate condition, still exemplified by many
primitive s t r e p s i r h i n e s , has a cone-shaped face joined t o t h e anterior
cranial fossa a t i t s base. Widely separated o r b i t s are divided by an
impressive inter-orbital plate that i s continuous with the upper portion
of t h e maxillary and nasal bones. T h i s represents t h e outer, upper surface
of t h e cone. The more important structures c m p l e t i n g the cone l a t e r a l l y ,
i n f e r i o r l y and i n t e r n a l l y are t h e medial walls of the orbits, the hard
palate and connecting bones, e . g . , t h e palatine and maxilla. During
mastication, forces transmitted to t h e f a c i a l s k u l l probably cause t h e
face t o bend and, t o sane e x t e n t , t w i s t up against its moorings. Mach of
t h i s load i s probably d i s t r i b u t e d through t h e core of t h e cone. B u t , with
t h e molar t e e t h and t h e temporomandibular j o i n t and muscles of mastication
positioned l a t e r a l l y , the p o s t o r b i t a l bar w i l l a l s o probably be affected
( s e e Endo, 1973: Roberts, 1979). The bar, being a T-shaped member connecting the f r o n t a l hone to the m a x i l l a and temporal through the s t r u t - l i k e
processes of t h e zyqomatic, must a l s o be loaded.
What i s being proposed, i n simple terms, i s
The contrasting anthropoid pattern is b u i l t around a greatly narrowed
central cmplex, and a lower, recessed face ( F i g s , 4,5). The reduced
nasal fossa and convergent orbits produce a r e l a t i v e l v narrow interorbi turn,
eliminating the broad wedge between the eye sockets aid reducing t h e
capacity of t h i s c r a n i o f a c i a l junction t o r e s i s t any twisting of the face
upon the braincase. The m e d i a l o r b i t a l walls are more c l o s e l y spaced and
are less e f f e c t i v e i n bracing against l a t e r a l forces. The entire face
tends to be tucked i n below the f r o n t a l bone, making t h e toothrows more
n e a r l y perpendicular t o the line of action of masseter and much of
Rosenberger: The Anthropoid Transition
80
temporalis. The upper, lateral, aspect of t h e f a c e i s completely s u t u r e d
t o the s i d e w a l l of the cranium by t h e o s s i f i e d p o s t o r b i t a l septum, Thus,
the a n t h r o p o i d face i s e s s e n t i a l l y hung from t h e neurocranium by a s e r i e s
of p a r a l l e l p i l l a r s formed by t h e t h i n p l a t e s of t h e interorbitum and t h e
postorbital septa.
Having a f u l l y fused mandibular symphysis, a n t h r o p o i d s may transmit
r e l a t i v e l y l a r g e amounts of force to t h e mandible and, presumably, t h e
rest of t h e masticatory periphery, i n comparison w i t h s t r e p s i r h i n e s ( s e e
Hylander, 1979b for a c o n t r a s t between Macaca and G a l a g o ) . With e n l a r g e d ,
r e l a t i v e l y vertical i n c i s o r s , and premolars e f f e c t i n g relatively l a r g e
amounts of r e s i s t a n c e by virtue of t h e i r i n c r e a s e d crushing-grinding
s u r f a c e a r e a , t h e p a t t e r n of forces absorbed by the face of an a n t h r o p o i d
may be assumed to be d i f f e r e n t from t h a t seen i n s t r e p s i r h i n e s . These
d i s t i n c t i o n s are exaggerated because s t r o n g facial loadings occur
a n t a g o n i s t i c a l l y , and i n unison. With a f u s e d symphysis, t h e jaw can be
powered by muscles on both sides of the head (Hylander, 1984) wfthout
d i s s i p a t i o n of force through twisting of an open j o i n t a t t h e f r o n t of
5. Schematic f r o n t a l s e c t i o n of h y p o t h e t i c a l euprimate
( l e f t ) and a n t h r o p o i d ( r i g h t ) skulls a t the c r a n i o f a c i a l j u n c t i o n ,
i . e . , near o p t i c foramen. The large n a s a l fossa acts a s a c e n t r a l
core of the face, b r a c i n g i t against t h e neurocranium. The
narrow i n t e r - o r b i t a l septum, a c o n s e q u e n c e of olfactory reduct i o n and o r b i t a l convergence i n preadapted omomyids, is l e s s
able to r e s i s t t w i s t i n g of t h e face about a c e n t r a l axis, as
when m a s s e t e r i s active and the z y g m a t i c i s t e n s e d against the
r e s i s t i n g food and temporo-mandibular j o i n t . The postorbital
p l a t e i s a l a t e r a l p i l l a r which compensates for loss of central
stability,
Fig.
- sepru
ANTHROPOID
R o s e n k r g e r : The Anthropoid Transition
81
the lower j a w (e.g. Beecher , 1979) t h u s making p a r a s a g i t t a l b i t e p o i n t s
more e f f i c i e n t . I n the anthropoids. t h e r e f o r e , l o a d s can be concentrated
at the f r o n t of the f a c e . With a f u s e d symphysis, c o n t r a l a t e r a l b i t i n g
forces would be resisted by the p a r a l l e l p i l l a r s a t the c r a n i o f a c i a l
junction.
In t h i s model t h e p o s t o r b i t a l p l a t e i s viewed as a mainstay i n the
connection of c r a n ~ a lcomponents, resisting t h e tendency t o t w i s t t h e face
about t h e narrow c e n t r a l i n t e r o r b i t a l strut. Due t o t h e fused a n t h r o p o i d
syn~uhysis, c o n t r a c t i o n of t h e rnassewr (wllich ,-lr.:i ses along the lower
border of the z y g m a t i c a r c h ) w i l l produce a large t e n s i l e component i n
t h e p o s t o r b i t a l bar, t e n d i n g t o separate i t from t h e f r o n t a l a t t h e i r
s u t u r e . By i n c r e a s i n g t h e l e n g t h of the s u t u r e and, more i m p o r t a n t l y ,
adding a perpendicular extension t h a t connects the postorbital bar t o
t h e s i d e w a l l of t h e s k u l l , i n c r e a s i n g t h e s i z e of the z y q m a t i c bone and
giving i t mechanical s u p p o r t , the tendency t o p u l l or rotate the l a t e r a l
p i l l a r out of position is counteracted. The a d d i t i o n of a t h i r d , inferiorly
placed, s u t u r e ( i . e . t h e zygmaticcknaxillary) adds mechanical integrity
t o t h e zygmatic p l a t e . Thus, postorbital c l o s u r e braces t h e f a c i a l skull
a g a i n s t t w i s t i n g produced by the system and reinforces t h e o r i g i n of the
m a s s e t e r muscle against enlarged forces.
The d e n t i t i o n i s an important source of vibration. me z y g m a t i c a r c h ,
under the bending i n f l u e n c e s of t h e masseter, and the articular surface
of t h e tempormandibular joint, which i s h e a v i l y loaded by t h e condyle
(Hylander, 1979a) l i k e w i s e contribute bone v i b r a t i o n . The transmission of
such bone conducted sounds t o the h e a r i n g mechanism v i a t h i s h e a v i l y
sutured and braced znthropoid s k u l l must be i n s u l a t e d , p o s s i b l y by t h e
developnent of porous, spongy bone i n t h e p e t r o s a l ( c f . Fleischer, 1979).
Some c m p a r a ~ i v eexamples may be cited i n support of the h i r p o t h e s i s t h a t
n o v e l loading conditions influence a s e l e c t i o n a l r e s p o n s e in the postorbita: bar of s t r e p s i r h i n e s , which by e x t e n s i o n suggests t h a t similar
processes could have d i r e c t e d t h e e v o l u t i o n of f u l l p o s t o r b i t a l closure,
For example, i n Loris the orbits are extremely convergent and supporting
c e n t r a l elements are correspondingly reduced. A s compensation for t h e
consequent reduction i n static stability, the p e r i p h e r a l elements of the
face a r e m o d i f i e d . The diameters of t h e l a t e r a l maxillary process,
i n f e r i o r and l a t e r a l a s p e c t of t h e -postorbital b a r and zyqomatic
arch are
-.
a l l e n l a r g e d t o i n c r e a s e t h e i r resistance against bending. In Hadropithecus, t h e fused mandibular symphysis increases the m a s t i c a t o r y canponent
of c o n t r a l a t e r a l forces and adds t o t h e amount of t e n s i o n borne by the
zygomatic a r c h v i a the m a s s e t e r . The arch and lateral o r b i t a l p i l l a r a r e
consequently g r e a t l y strengthened. A similar condition occurs in Adapis,
which also has a fused symphysis, although i t retains the p r i m i t i v e
elongate snout,
explanations have been given f o r t h e evolution of Lhe posto r b i t a l p l a t e . C a r t m i l l (1980) lists five: ( L ) support o f t h e eye,, ( 2 )
protection of t h e eye, ( 3 ) increased attachment f o r a n t e r i o r t e m p o r a l i s ,
( 4 ) b r a c i n g the eye and o r b i t a g a i n s t tension from m a s t i c a t o r y muscles,
A number of
82
Rosenberger: The Anthropoid Transition
and ( 5 ) i n s u l a t i o n o f t h e f o v e a t e y e f r o m t e m p o r a l i s c o n t r a c t i o n s ( s e e
Figure 6 ) . These i n t e r p r e t a t i o n s have been v a r i o u s l y applied to the posto r b i t a l p l a t e of anthropoids (2,3,5), t h e enlarged p o s t o r b i t a l bar of
t a r s i e r s ( 1 . 5 ) and the u n e n l a r g e d bar of ancestral euprimates ( 2 , 4 ) .
Perhaps the b e s t developed arguments proposed i n recent years are those
given by Cachel (1979) and Cartmill (1980). Cachel e x p l a i n s the anthropoid
condition as an a d a p t a t i o n t o increase t h e s u r f a c e of attachment f o r t h e
anterior temporalis, thought t o be e s p e c i a l l y u s e f u l i n incisivation.
C a r t m i l l (1930) suggests t h a t t h e e x p l a n a t i o n for the morphology i n
tarsiers
anthropoids i s t h a t p o s t e r i o r closure o f t h e o r b i t i s n e c e s s a r y
t o keep the fovea bearing eyeball from o s c i l l a t i n g a s temporalis c o n t r a c t s
d u r i n g chewing. The m o d e l proposed above i s compatible w i t h C a c h e l ' s hypothesis, though it emphasizes different factors. It is markedly different
from Cartmill's, i n p a r t because o u r i n t e r p r e t a t i o n s of t a r s i e r affinities
are mutually e x c l u s i v e .
Fig. 6. Six t h e o r i e s f o r the evolution of t h e postorbital septum:
(a]e y e b a l l protection; ( b ) a t t a c h m e n t surface for a n t e r i o r
temporalis; (c)eyeball support i n t a r s i e r s ; (d)i n s u l a t i n g the
foveate e y e b a l l from oscillating with temporalis activity;
(elresisting bending under muscular t e n s i o n ; ( £ ) b r a c i n g the
f a c i a l s k u l l against t w i s t i n g and s e c u r i n g the masseter against
t h e non-rotating d e n t a r i e s .
(c)
eyeball
~ U O P O ~ I
Rosenberqer: The Anthropoid Transition
S u m a r y and conclusions
Anthropoids are a monophyletic subqroup of the Haplorhini.
The diphyly t h e o r y af anthropoid origins fails to address the contradictory
i m p l i c a t i o n s of shared d e r i v e d similarities found i n platyrrhines and
c a t a r r h i n e s . I n s t e a d , it focuses upon differences between t h e two qroups,
which have been considerably reduced by new information about the anatany
of t h e Oligocene African catarrhines. The diphyly theory is steeped i n
t h e g r a d i s t i c t r a d i t i o n of primatologi., which overemphasizes t h e possibilit i e s of p a r a l l e l i s m w i t h o u t f a l s i f y i n g t h e Darwinian null hypothesis t h a t
s i m i l a r i t y i n £ o m and f u n c t i o n i s an i n d i c a t i o n of affinity.
The c u r r e n t geographical s e p a r a t i o n of platyrrhines and c a t a r r h i n e s into
N e w and Old World realms postdates t h e emergence of the Anthropoidea. The
morphological evidence i n d i c a t e s t h a t catarrhines, of any s o r t , a r e t o o
d e r i v e d t o be d i r e c t ancestors of the p l a t y r r h i n e s , and hints a t the
p o s s i b i l i t y t h a t c a t a r r h i n e s have more p r i m i t i v e , extra-African relatives
i n the Indo-Pakistan r e g i o n . Such a relationship f a v o u r s L a u r a s i a a s the
g e o g r a p h i c a l s o u r c e f o r p r o t o a n t h r o p o i d s . Faywr p r i m a t e s are but one
e l e m e n t of a changing Tethyean mammalian fauna. South America s i m i l a r l y
absorbed v a r i o u s e a r l y T e r t i a r y mammals that found t h e i r way across t h e
t e c t o n i c a l l y - a c t i v e n u c l e a r Central America and proto-carribbean. S i n c e
the T e r t i a r y history of mannnals on both these southern c o n t i n e n t s mirrors
one another in pattern, the i n v o c a t i o n of a s p e c i a l circumstance, t h a t i s ,
a unique westward t r a n s a t l a n t i c d i s p e r s a l , is not n e c e s s a r y t o explain the
d i s j u n c t i o n of the anthropoids.
Anthropoids are probably the descendants of a h a p l o r h i n e a n c e s t r a l stock
t h a t would nominally be c l a s s i f i e d a s omomyid. The l a t t e r were widespread
i n L a u r a s i a d u r i n g t h e Eocene and included c r a n i a l a n d d e n t a l morphs
s u f f i c i e n t l y p r i m i t i v e t o be a n c e s t r a l t o t h e h i g h e r primates. T a r s i i d s
a r e an u n l i k e l y sister taxon because they a r e h i g h l y autapomorphous and
t h e y are probably related t o a different omomyid subgroup. Non-primitive
s i m i l a r i t i e s s h a r e d w i t h anthropoids tend t o be convergences. Adapids are
probably the early members of t h e greater l e m u r i f o m c l a d e , a modified
g r a u p s h a r i n g no Immediate ancestry w i t h h a p l o r h i n e s a f t e r t h e d i f f e r e n t i a t i o n of each from a n c e s t r a l euprimates. A few adapids have apparently
converged upon anthropoids, l e a d i n g sme t o conclude that t h e y a r e possibly
anthropoid ancestors.
The a n t h r o p o i d t r a n s i t i o n w a s a d a p t i v e l y predicated upon a h a p l o r h h e
cranial morphology, t y p i f i e d by such features as an a b b r e v i a t e d , l o w face,
a s m a l l n a s a l cavity and c r a n i o f a c i a l h a f t i n g along a narrow i n t e r o r b i t u r n .
Reinforcement of the c r a n i o f a c i a l junction by t h e development of a postorbital plate enabled the anthropoid s k u l l t o a b s o r b e c c e n t r i c loads t h a t
tend t o t w i s t the face up a g a i n s t t h e neurocranium, t o apply powerful
b i t i n g f o r c e with the i n c i s o r s and premolars, t o secure the zygomatic bone
a g a i n s t t h e tension of masseter, and t o t r a n s f e r forces across t h e fused
mandibular symphysis t o e i t h e r s i d e of t h e f a c e and toothrows. The
p n e u m a t i z a t i o n of t h e p e t r o s a l bone may serve t o i n s u l a t e the hearing
mechanism from vibrations t r a n s m i t t e d through t h e more solidly fused
anthropoid head. Thus, t h e a d a p t i v e s h i f t of t h e masticatory a p p a r a t u s
was probably r e l a t e d t o a critical r e l i a n c e upon resistant fruits, such as
Rosenberger: The Anthropoid Transition
84
legumes (with t h e i r hard c o v e r i n g s ) and seeds, when less c o s t l y f r u i t s
were u n a v a i l a b l e . Additional shared derived f e a t u r e s of a n t h r o p o i d s help
t o delineate t h e o t h e r dimensions of t h e i r formative e c o l o g i c a l n i c h e and
many of t h e s e are unrelated t o feeding. For example, t h e coordination of
a r e l a t i v e l y large brain w i t h acute v i s i o n made possible the coding of a
huge amount of v i s u a l information stemming frm t h e environment, which
far exceeded t h e amount of 'smell' d a t a cues that l e m u r i f o m s or primitive
euprimates could e x t r a c t . The sheer c o g n i t i v e advantages of e a r l y anthropoids should not be ignored i n models d e t a i l i n g their mode of origin.
By drawing t o g e t h e r the approaches of p h y l q e n e t i c r e c o n s t r u c t i o n and
functional analysis, r a t h e r than p e r p e t u a t i n g t h e f a l s e dichotcwy t h a t
has d i v i d e d them i n s y s t e m a t i c endeavours, f u t u r e work will add clarity
to discussions on the major topics of anthropoid evolution. More pointed
t e s t s of h m o l o g y , and more s a t i s f a c t o r y interpretations of character
polarity, should help generate powerful heuristic models of t h e adaptive
t r a n s i t i o n that r e s u l t e d i n Anthropoidea, and the separate r a d i a t i o n s of
the New and O l d World l i n e a g e s . I f the f o s s i l record continues t o grow as
~t has done r e c e n t l y i n both hemispheres, the next decade of research on
p l a t y r r h i n e s , c a t a r r h i n e s and t h e anthropoid transition w i l l prove even
more rewarding tham the past c e n t u r y of excitement, discovery and controversy.
Acknowl edgements
Jack Prost and E r i c Delson contributed importantly t o sane of
t h e ideas expressed in this paper, f o r which I am g r a t e f u l , I acknowledge
support frmn t h e National Science Foundation, BNS 810359, t h e O f f i c e s of
S o c i a l Science Research and of Sponsored Research, U I C , f o r financial
a s s i s t a n c e . The illustrations w e r e drawn by L o r i Groves and R a y Brod.
S t e l l a W r i g h t s e l l , Kathleen Rizzo and C a t h e r i n e Becker helped me canplete
t h e manuscript.
References
K e y references
(1980). M o r p h o l q y , f u n c t i o n and e v o l u t i o n of the a n t h r o p o i d
p o s t o r b i t a l septum. I n : Evolutionary Biology of the New World
and Continental D r i f t , eds., X.L. Ciochon and A . B . C h i a r e l l i ,
pp. 243-74. N e w York, Plenum Press.
Gregory, W.K.
(1920). On the structure and relations of Notharctus, an
American Eocene primate. Mem. Am. Mus. N a t . Host., New s e r i e s
3 , 49-243.
H o f f s t e t t e r , R.
(1980). Origin and deployment of New World monkeys
emphasizing the southern continents route. I n E v o l u t i ~ f l a r y
Biology of the New World Monkeys and Continental Drifts, e d s . ,
R.L. Ciochon and A.B. Chiarelli, pp. 103-22. New York, Plenum
Press.
Le Gros C l a r k , W.E.
(1963). The A n t e c e d a n t s of Man. 2 ed. New York, Harper
C a r t m i l l , M.
& ROW.
Rosenberger: The Anthropoid Transition
85
& S z a l a y , F.S.
(i980). On the t a r s i i f o m o r i g i n s of
A n t h r o p o i d e a In: Evolutionary Biology of t h e New World Monkeys
and Continental D r i f t . , pp. 139-57, N e w York, P l e n u m Press.
R o s e n b e r g e r , A.L., Strasser, E. & D e l s o n , E .
(1985). The a n t e r i o r d e n t i t i o n of N o t h a r c t u s a n d t h e adapid-anthropoid hypothesis. F o l i a
p r i m a t o l . , 4 3 , 15-39.
Rosenberger, A.L.
Main References
:1927). The Anatomy of t h e common marmoset (Hapale jacchus
Kuhl) . Proc. 2001. Soc. Lond. , 593 -718.
Beecher, B.M.
{1979). F u n c t i o n a l s i q n i f i c a n c e of t h e m a n d i b u l a r s p p h y s i s .
J. Morph. , 159, 117-30.
Bown, T . M . & Sirnons, E.L.
( 1 9 8 4 ) . First record of marsupials e eta the ria:
Polyprotodonta) from the O l i g o c e n e i n Africa. Nature 308, 447-9.
C a c h e l , S.M.
( 1 9 7 9 ) . A f u n c t i o n a l analysis of the p r i m a t e masticatory
system and t h e o r i g i n of anthropoid p o s t - o r b i t a l septum. Am. J.
Phys. Anthrop., 50, 1-17.
Cachel, S .
(1981). P l a t e tectonics and the problem of anthropoid o r i g i n s .
Yrbk. Phys. Anthrop., 2 4 , 139-72.
C a r t m i l l , M.
(1982). Basic primatology and prosimian e v o l u t i o n . rn A
H i s t o r y of American P h y s i c a l A n t h r o p o l q y , ed. F. Spencer,
pp. 147-86. New York: Academic Press.
C a r t m i l l , M. & Kay, B.F.
(1978). C r a n i d e n t a l morphology, t a r s i e r a f f i n i t i e s
and primate sukarders. I n Recent Advances i n P r i m a t o l o g y
m o l u t i o n , (eds.) C h i v e r s , D. J. & Joysey, K.A., PP- 205-14London: Academic Press.
C a r t m i l l , M,, M a c P h e e , R.D.E. & Simons, E.L.
(1981). Anatomy of t h e
temporal bone i n early anthropoids, with remarks on the problem
of anthropoid o r i g i n s . A r n . J. Phys. ~ n t h r o p . 5 6 , 3-21.
Ciochon, R.L. & C h i a r e l l i , B. (1980j. Evolutionary Biology of New World
Monkeys and C o n t i n e n t a l D r i f t . New York: Plenum P r e s s .
Cooke, H . B . S .
(1972).
The fossil m m m a l fauna of Africa. I n E v o l u t i o n ,
M m a l s , and Southern C o n t i n e n t s , eds. A. Keast, F.C. Erk &
B. G l a s s , pp. 89-139. Albany: State U n i v e r s i t y of N e w York
Press.
Dagosto, M.
(1985). The d i s t a l t i b i a of primates with s p e c i a l reference
t o the omanyidae. I n t . J. Primatol., 6 45-75.
D a r w i n , C.
( 1 8 7 1 ) . The Descent of Man. London: Murray.
Delson, E . D .
Rosenberger, A.L.
(1980). P h y l e t i c perspectives on p l a t y r r h i n e origins and anthropoid r e l a t i o n s h i p s . I n Evolutionary
B i o l o g y of New World Monkeys and c o n t i n e n t a l D r i f t , eds.
R . L . Ciochan & ~ h i a r e l l i ,A . B . , pp. 445-58.
Delson, E. & R o s e n b e r g e r , A.L.
(1984). Are there any anthropoid primate
" l i v i n g f o s s i l s " ? I n L i v i n g Fossils, e d s . N . Eldredga &
S . S t a n l e y , pp. 50-61. N e w York: Springer-Ver lag.
Elliot-Smith, G.
( 1 9 2 4 ) . The E v o l u t i o n of Man, London: O x f o r d Univ. P r e s s
Endo, B.
(1973). S t r e s s a n a l y s i s o n the f a c i a l skeleton of gorilla by
means of t h e wire s t r a i n gauge method. Primates, 2 4 , 3 7 - 4 5 .
Beattie, J.
86
Rosenberger : The Anthropoid Transit i o n
(1980). Comparative s t u d y of t h e endocranial c a s t s of New and
O l d World monkeys.
E v o l u t i o n a r y B i o l o q 7 of New World Monkeys
and C o n t i n e n t a l D r i f t , eds. R.L. Ciochon & C h i a r e l l i , A.B.
pp. 275-92. New York: Plenum Press.
F l e a g l e , J.G. & Bown, T.M.
(1983). New primate fossils f r m Late Oligocene
(Colhuehaupian) l o c a l i t i e s of Chubut Province, A r g e n t i n a , Folia
p r i m a t o l q i a , 41, 240-266.
F l e a g l e , J . G . L Rosenberqer, A.L.
( 1 9 8 3 ) . C r a n i a l rnorpholqy of the e a r l i e s t
anthropoids.
Morphologie, E v o l u t i o n , ~orphogengsed u Crane
et ~ n t h r o ~ o ~ e n & pp.
s e , 141-53. P a r i s : Centre National de l a
Recherche Scientifique.
F l e i s c h e r , G.
(1978). E v o l u t i o n a r y principles of t h e mammalian middle e a r ,
Adv. Anat. Embryol. Cell. B i o l . 55, 1-69.
Flower, W.H.
(1866). An Introduction t o t h e Osteology of the Mammalia.
Amsterdam: A. Asher & Co.
Ford, S.M.
(1980). C a l l i t r i c h i d s as p h y l e t i c dwarfs, and the place of the
Callitrichidae i n P l a t y r r h i n i . Primates, 2 1 , 31-43.
Gecffrwy, S a i n t - H i l a r e , E.
( 1 8 1 2 ) . Tableau des quadrumanes, I. Ord.
Quadrumanes Ann. do Mus. d'Hist. Nat., P a r i s , 19, 85-122.
Gingerich, P.D.
(1975). A new genus of Adapidae (Mammalia,Prirnates) from
t h e l a t e Eocene of s o u t h e r n France and i t s significance f o r
t h e o r i g i n of h i g h e r primates. Contrib. Mus. Paleontol. Univ.
Michigan, 2 4 , 163-70.
G i n g e r i c h , P.D.
( 1 9 7 7 ) . Radiation of Eocene Adapidae in Europe. Geobios,
Mem. s p . 1 , 165-82.
Gingerich, P . D .
(1980). Eocene Adapidae, p a l e o b i q e o g r a p h y , and the o r i g i n
of South American P l a t y r r h i n i . I n E v o l u t i o n a r y Biology of New
World Monkeys and Continental D r i f t , eds, R . L . Ciachon a
A.B. C h i a r e l l i : pp. 123-38. New York: Plenum P r e s s .
Gingerich, P.D.
(1981). Early Cenozoic Cknomyidae and t h e e v o l u t i o n a r y
history of t a r s i i f o r m primates. J . Hum. Evol., 10, 345-74.
Gray, J . E .
(1821). On the n a t u r a l arrangement of vertebrose a n i m a l s .
London Med. Repast. 1 5 . 296-310,
G r o v e s , C.?.
( 1 9 7 2 ) . Phylogeny a n d c l a s s i f i c a t i o n of primates. In Pathology
of Simian Primates-Part I, ed. R . F i e n n e s , pp. 11-57. B a s e l ,
Karger.
Haeckel, E.
(1899). The L a s t L i n k . London: BLack.
Huxley, T.H.
(1863). Evidence a s t o Man's Place i n Nature. London:
W i l l i a m s ti Norgate.
Hylander, W.L.
(1979a). An experimental analysis of temporanandibibular
j o i n t r e a c t i o n force in macaques. Am. J, Phys. Anthrop. 51,
433-55.
Hylander, W.L.
(1979b). Mandibular function i n Galago c r a s s ~ c a u d a t u s and
Macaca f a s c i c u l a r i s : an i n v i v o approach to stress analysis
of the mandible. J . Morph., 1 5 3 , 253-96.
Hylander, W.L.
(1984). Stress and s t r a i n in t h e mandibular symphysis of
primates: A test of competing hypotheses. Am. J. Phys. Anthrop.,
64 , 1-47,
Kay, R.F.
(1977). The evolution of.molar occlusion i n the Cercopithecidae
and early catarrhines. Am. J. Phys. A n t h r o p . , 4 6 , 327-52.
Falk, D.
Rosenberger: The Anthropoid Transition
87
( 1 9 8 0 ) . P l a t y r r h i n e origins: a c r i t i c a l reappraisal of t h c
d e n t a l e v i d e n c e . In E v o l u t i o n a r y B i o l o g y o f New World Monkeys
and C o n t i n e n t a l D r i f t , e d s . R . L . Ciochon a A . B . Chiarelli,
pp. 159-88. New York: Plenum Press.
Kay, R . F . & Hiiemae, K.M.
(1974)
Jaw m w e m e n t and tooth u s e i n r e c e n t and
f o s s i l primates. Am. J. Phys. Anthrop. 40, 227-56.
Kay, R.F. & Simons, E.L.
( 1 9 8 3 ) . Dental fornlulae and d e n t a l e r u p t i o n
p a t t e r n s i n P a r a p i t h e c i d a e ( P r i m a t e s , h n t h r u p o i d e a ) . Am. J .
Phys. Anthrop. 6 2 , 363-76.
K e i t h , A.
(1934). The C o n s t r u c t i o n of Man's Family Tree. London: W a t t s &
Kay, R . F .
.
co.
h v o c a t , R.
(1980). The i m p l i c a t i o n of r o d e n t paleontology and biogeography
t o t h e g e o g r a p h i c a l s o u r c e s and o r i g i n of platyrrhine primates.
I n E v o l u t i o n a r y Biology of New World Monkeys and C o n t i n e n t a l
Drift, eds. R.L. Ciochon and A . B . C h i a r e l l i , pp. 93-102. New
York: Plenum P r e s s .
Contributions t o the extinct v e r t e b r a t e fauna of t h e
Geol. S u m . T e r r . (hayden) I .
Le Gros C l a r k , W.E. (1934). Early F o r e r u n n e r s of Man. B a i l l i e r e , London.
Luckett, W. P. ( 19BO)
Monophy l e t i c o r d i p h y l e t i c origins of Anthropoidea
and Hystricognathi: I n E v o l u t i o n a r y B i o l o g y of New World
Monkeys and C o n t i n e n t a l D r i f t , eds. R.L. Ciochon & A . B .
C h i a r e l l i , pp. 347-68. New York: Plenum.
(19731 Clades versus grades in primate
L u c k e t t , W . P . & Szalay, F.S.
Evolutionary Relationships Among R d e n t s . New York: Plenum
Press.
(1978). Clades v e r s u s grades i n primate
L u c k e t t , W.P., S z a l a y , F.S.
phylogeny. I n Recent A d v a n c e s in P r i m a t o l q y , Vol. 3 E v o l u t i o n .
& s . D.J. Chivers & K.A. Joysey, pp. 2 2 8 - 3 7 , New York: Academic
press.
MacFadden, B . J .
(1980). R a f t i n g m a m m a l s o r drifting i s l a n d s ? : b i o g e q r a p h y
of the greater a n t i l l e a n i n s e c t i v o r e s Nesophontes and S a l e n d o n .
J. Biogeography, 7 , 11-22.
MacPhee, R.D.E.,
C a r t m i l l , M. & G i n g e r i c h , P.D.
( 1 9 8 3 ) . P a l e q e n e primate
b a s i c r a n i a and the d e f i n i t i o n of t h e o r d e r Primates. Nature,
London, 3 0 1 , 509-11.
Marshall, L.G., P a s c u a l , R., C u r t i s , G.H.
( 1 9 7 7 ) . South American Geochronology: Radicanetric Time S c a l e for Middle t o L a t e T e r t i a r y
Mammal-bearing Horizons i n P a t a g o n i a . S c i e n c e , 195, 1 3 2 5 - 2 9 .
Martin, R. D.
(1973 )
Comparative anatomy and primate s y sternatics. S p p .
2001. Soc. Lond. 3 3 , 301-37,
McKenna, M.D.
( 1 9 8 0 ) . Early h i s t o r y and biogeography of South America's
e x t i n c t l a n d mammals. I n E v o l u t i o n a r y Biology of N e w World
Monkeys and C o n t i n e n t a l D r i f t , eds. R . L . Ciochon & A.B.
Chiarelli, gp. 4 3 - 7 7 . New York: Plenum Press.
M a t t h e w , W.D.
(1915)
Climate and e v o l u t i o n . Ann. New York, Acad. S c i :
2 4 , 171-3J8. Reprinted ( 1 9 39) as s p e c i a l P u b l . New York Acad.
S c i . , 1.
Mayr, E. ( 1 9 8 2 ) . The Growth of Biological Thought. Cambridge, Mass.
Belknap P r e s s .
M i v a r t , S t . George,
(1874). Man and Apes. New York: D. Appleton & C o .
Leidy, J.
(1873).
Western Territories. Rep. U . S .
.
.
.
.
Rosenberger : The Ant hromid T r a n s i t i o n
88
Sarmiento, E.E.
(1984). External and middle ear c h a r a c t e r i s t i c s of primates, with reference to t a r s i e r - a n t h r o p o i d
a f f i n i t i e s . Am. Mus. Novitates, 2787, 1-23.
Roberts, D.
(1979). Mechanical structure and f u n c t i o n of the c x a n i o f a c i a l
s k e l e t o n of the domestic dog. Acta a n a t . , 103, 4 2 2 - 3 3 .
Rosenberger , A. L. (i981a). A mandible of B r a n i s e l l a boliviana
(Platyrrhini,
Primates) from t h e Oligocene of South America. I n t . J. P r i m a t o l .
2 , 1-7.
R o s e n k r g e r , A.L.
(1981b). Systematics: the higher t a x a . In Ecolcqy and
Behaviour of Neotropical Primates, eds. A.F. Coimbra-Filho and
R . A . M~ttermeier,pp. 9-27. Rio de Janeiro: Academia B r a s i l i e r a
de C i e n c i a s .
Rosenberger, A . L .
(1983). Aspects of the systematics and evolution of
the marmosets. In A Primatoloqia No. B r a z i l , ed. M.T. de Mallo,
pp. 159-80. B e l o Horizonte: UFMG.
Rosenberger, A . L . & Kinzey, W.G.
(1976). ~unctionalp a t t e r n s of molar
occlusion in p l a t y r r h i n e primates. Am. J . Phys. Anthrop., 4 5 ,
281-98.
Rosenberger, A.L. & Strasser, E.
(1985). Toothcomb o r i g i n s : Support f o r
the grooming hypothesis. Primates.
Savage, D.E. & Russell, D.E.,
(1983) Mammalian Paleofaunas of t h e World:
London: Addison-Wesley P u b l i s h i n g C o .
Schultz, A.H.
(1969). The L i f e of Primates. N e w York: Universe Books.
Simons, E . L .
(1972). Primate Evolution: An I n t r o d u c t i o n t o M a n ' s P l a c e
i n Nature. New Y o r k : MacMillan.
Sirnpson, G.G.
(1961). P r i n c i p l e s of Animal Taxonomy. New York: C o l u m b i a
Univ. P r e s s .
Sykes, L.R., McCann, W.R. & Kafka, A.L.
( 1 9 8 2 ) . Motion of Caribbean plate
during last 7 million years and implications for earlier
Cenozoic movements. 3 . Geophys. Res. 87, 10,656-76.
Szalay, F.S. & Delson, E.
(1979). Evolutionary History of the P r i m a t e s ,
New York: Academic Press.
Tarling, D.H.
(1980). The geologic e v o l u t i o n of South America w i t h special
reference t o the last 2 0 0 million years. In E v o l u t i o n a r y Biology
of t h e New World Monkeys and C o n t i n e n t a l Drift, eds. R . L . Ciochon
and A.B. C h i a r e l l i , pp. 1 - 4 1 . New York, Plenum Press.
Wallace, A.R.
( 1 8 7 6 ) . The G e q r a p h i c a l D i s t r i b u t i o n of Animals. 2 Vols.
London: MacMillan.
W o d Jones, F.
(1929). Man's Place Among the Mammals. London: Edward
Arnold & Co.
Wortman, J.L.
(1903-04). Studies of Eocene Marnmalia i n t h e Marsh Collection,
Peabody Museum. Part 2. Primates. A m e r . J. Sc., S e r . 4, 1 5 ,
163-76, 399-414, 419-36; 16, 345-68; 1 7 , 2 3 - 3 3 , 133-40, 203-14.
Packer, D .
&
.