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Morphology-based systematics (MBS) and problems with fossil hominoid and hominid systematics.

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DOI 10.1002/AR.10055
Morphology-Based Systematics (MBS) and
Problems With Fossil Hominoid and Hominid
The generalized/primitive nature of the hominoid dentition and often fragmentary nature of fossils, coupled with
enthusiastic optimism for making revolutionary finds, has wreaked havoc with recognition of early human ancestors
and reconstruction of fossil hominoid phylogeny. As such, the history of paleoanthropology is one of repeated
misidentification of fossil ancestors and of occasional fraud. Although this history has led many workers to lose
confidence in morphology based systematics (MBS), past and present misidentifications are actually due to a
disregard of systematic methodology. Systematics depends on the continuity of life and gains its objectivity largely
from the order alpha taxonomy imposes on morphologic discontinuities in closely related taxa (i.e., species and
genera). Transformation of characters fixed in species into character complexes, as manifested in taxa nested at
different levels of relationship, form the foundation for higher-level taxonomy and for phylogeny. Because in most
cases, hominoid fossils are unable to provide the data needed to resolve alpha taxonomy, classification and
phylogeny of fossil taxa must be guided by analogies to living taxa. Hominid and hominoid fossil taxonomy and
phylogeny, however, has been based largely on preevolutionary notions and on misinterpretations of the polarity of
assumed diagnostic characters. More often than not, fossils lack resolution for the taxonomic level or rank they are
assigned to and taxa are erected without appropriate analogies to living forms. As such, phylogenies based on these
classifications are unlikely to be correct. More in-depth anatomical studies that are in accordance with systematic
methodology are likely to hold the key to correctly classifying fossils and unraveling hominoid and hominid phylogeny.
Anat Rec (New Anat) 269:50 – 66, 2002. © 2002 Wiley-Liss, Inc.
KEY WORDS: systematics; fossils; evolution; misidentification; taxonomic level; Alpha taxonomy; morphology; phylogeny;
cladistics; comparative anatomy; paleoanthropology
One of the main tasks of paleoanthropology is to classify fossil
hominid remains, and unravel their
phylogeny. As a long-established science, morphology based systematics
(MBS) has provided effective tools for
accomplishing this task. The primitive/generalized nature of the hominoid dentition and the often-fragmenDr. Sarmiento is Research Associate in
the Division of Vertebrate Zoology,
American Museum of Natural History
(AMNH). Dr. Stiner is a Scientific Assistant in the Division of Vertebrate Zoology at AMNH. Dr. Mowbray is Collections Associate in the Division of
Anthropology at AMNH.
*Correspondence to: Esteban E. Sarmiento, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024. E-mail:
© 2002 Wiley-Liss, Inc.
tary nature of fossils (Sarmiento,
1987), both coupled with enthusiastic
optimism for making revolutionary
finds, have played havoc with the recognition of early human ancestors
and reconstruction of fossil hominoid
phylogeny (see Walker, 1969; Pilbeam, 1970, 1972; Simons, 1965,
1972; Szalay and Delson, 1979; Begun, 1992; Conroy et al., 1992; White
et al., 1994).
On the basis of fossil evidence, the
human lineage until recently was believed to extend back to the middle to
late Miocene (Keith, 1915; Simons,
1967, 1972; Leakey, 1967, 1968; Pilbeam, 1968, 1969, 1970). Gorillas and
chimpanzees were envisioned to be
separate lineages in the early Miocene
(Proconsul major [gorilla]; Walker and
Rose, 1968; Simons and Pilbeam, 1965;
Pilbeam, 1969; and Proconsul africanus
[chimpanzee] Pilbeam, 1969), and great
apes (Aegyptopithecus; Simons, 1965,
1972) and purported hominids (Propliopithecus; Schlosser and von Zittel, 1923;
Gregory, 1934; Simons, 1963; Pilbeam,
1967, 1968) were believed to appear
during the Eocene or near the EoceneOligocene boundary (Osborn, 1922;
Kappelman et al., 1992; Van Couvering
and Harris, 1993). For nearly four decades, most paleoanthropologists regarded the doctored remains of Piltdown as the earliest human ancestor
(Woodward, 1917; Eliott-Smith, 1924;
Keith, 1934, 1940; Oakley and Hoskins,
1950; Oakley, 1952). Yet, they were initially unwilling to recognize the possibility that the South African australopithecines (Keith, 1925, 1940; EliottSmith, 1925; Woodward, 1925) and the
Trinil remains (Virchow, 1895) were
When more fossil material became
known and more sober assessments
were made, none of the early hominoid phylogenetic claims were supported, and in retrospect, some seem
absurd (Gingerich, 1973; Sarmiento,
1987, 1995; Pilbeam et al., 1990). Piltdown was exposed to be a hoax constructed from the doctored remains of
a modern human and an orangutan
(Weiner et al., 1953; Weiner, 1955).
Thereabouts, australopithecines became widely accepted as early human
ancestors with little objective evaluation (Mayr, 1950; Le Gros Clark,
1950a,b, 1955; Oakley, 1954; Von Koenigswald, 1956; Simpson, 1963; Robinson, 1954, 1962, 1965).
The rapidly changing behavioral
and morphologic interpretations of
the hominoid fossil record that have
since ensued have caused considerable confusion among paleoanthropologists (Larson, 1998; Foley, 2001)
and have led many to lose confidence
in MBS (Chaline, 1999; Lockwood
and Fleagle, 1999; Wood and Collard,
1999; Collard and Wood, 2000). Partly,
this loss of confidence centers on the
very meaning of homology and the
inherent problems of identifying homologies and separating these from
parallelisms/convergences and reversals (collectively termed homoplasies;
Hall, 1994; Lieberman, 1999). This
has spurred a recent interest in turning from MBS toward biomolecular
analysis (Ruvolo et al., 1991, 1993,
1994; Pilbeam, 2000) or in couching
morphology based analyses within
(1) development (Lieberman, 1995;
Lieberman et al., 1996; McCollum,
1999, 2000), (2) phenetics (Howells,
1973, 1989), or (3) cladistic techniques based exclusively on fossils
and quantitative characters (Chamberlain and Wood, 1987; Lieberman et
al., 1996). Some paleoanthropologists
have suggested that phylogenetic
analyses should be based solely on
categories of skeletal limb characters
weighed according to their own interpretations of function and developmental patterns (see Lovejoy et al.,
1999, 2000). As a result, some workers
seem to suggest that systematics and
its progress are based more on general
consensus rather than the logical
organization of empirical evidence
(Franciscus, 1999). Past misinterpretations of the hominoid fossil evi-
dence, however, do not reflect the
shortcomings of MBS but have occurred mainly because of misunderstandings in its methodology and theoretical basis. This essay presents a
review of the reasoning underlying
MBS to (1) show its usefulness for
interpreting hominoid fossil evidence;
(2) explain past misinterpretations
and misclassification of fossils; and
(3) provide a framework that serves as
a guideline for future studies in hominoid systematics.
Because anatomical characters form
the foundation for vertebrate systematic studies and are useful for untangling relationships between taxa at all
levels of relatedness, anatomists stand
to make significant contributions to
hominoid and hominid systematics. It
is the overall goal of this essay to pro-
Past misinterpretations of
hominoid fossil evidence
do not reflect the
shortcomings of
morphology based
systematics but have
occurred mainly
because of
misunderstandings in its
methodology and
theoretical basis.
vide anatomists with both the tools and
the incentive to do so.
The moment one willingly accepts
that all living organisms share a common origin (Darwin, 1859; Huxley,
1895), the powers of systematic studies are obvious (Simpson, 1961; Mayr,
1963). At its lowest level, each taxon
serves as a natural experiment that
explores adaptive possibilities afforded to it by the environment and,
thus, reveals evolutionary processes.
Closely related species arrive at different solutions to environmental problems by using the inherent variation
in a largely shared phenotype. Thus,
studies of closely related species reveal the type of characters underlying
overall differences in phenotypic expression, and the anatomical regions
where these characters are found.
When linked to ecological data for
each member taxon, these studies
have the potential to reveal the associated environmental differences and,
thus, the variables bearing on speciation for the concerned taxonomic
group (Vrba et al., 1995; Sarmiento et
al., 1996; Sarmiento and Oates, 2000).
Examination of nested taxa with varying relationships at ascending levels
of classification provide insights into
how (1) initial characters marking
species divergence may become evolutionary trends, (2) evolutionary trends
may be molded through time into the
complex structures that define higher
taxonomic categories, (3) complex
structures once incorporated in ancestral lineages are subsequently
modified to best suit the needs of descendant taxa. Founded on the continuity of all life forms, systematics
assumes that existing morphologic
discontinuities in living (crown) taxa
at various levels of relatedness must
have been bridged by intervening
populations, which are presently extinct.
Alpha taxonomy is concerned with the
links among geographic distribution;
reproductive communality; speciation; relative evolutionary time; and
behavioral morphologic, and adaptive
differences in closely related taxa
(usually within the same genus). It
serves as the basis for systematics and
as the building blocks for all higherlevel taxonomy or phylogeny. Alpha
taxonomy bridges the gaps between
individuals, populations, and species
and strives to sort phenotypic variation due to sex, developmental age,
and environmental/habitat variables
(e.g., altitude, temperature, rainfall,
cloud cover, vegetation, etc.), arriving
at the limits of intraspecific variation.
It is therefore essential for identifying
those characters (behavioral, morphologic, or genetic) associated with reproductive and phenotypic discontinuity (i.e., distinctiveness) and for
distinguishing species-specific char-
Figure 1. Geographic distribution of individuals (dots) belonging to three populations. The red and yellow populations maintain their
distinctiveness in overlapping areas and are, thus, by definition different species. Without a range of overlap, there is no objective test to
decide whether blue and red populations are different species. This decision is in part subjective and depends on whether or not
magnitude of differences distinguishing the two is comparable to, or more than that distinguishing objectively determined species (i.e. the
red and yellow populations). Species determination for blue and yellow populations is also partly subjective. It depends on the magnitude
of differences between the two and the degree to which their hybrids show grading of diagnostic differences. A gradual cline with a wide
zone of hybridization between them suggests one species. A very abrupt cline with a narrow hybrid zone as shown here indicates different
acters from intraspecific variation
within a taxonomic group (Schuh,
2000). By exploring the minimum
differences representing reproductive
and phenotypic discontinuities, alpha
taxonomy allows the recognition of
characters and associated adaptations
that define closely related species and,
thus, the variables associated with
species divergence.
Species, and the characters that define them, may be objectively arrived
at based on whether or not distinct
populations maintain their distinctiveness in areas of sympatry (Fig. 1;
Simpson, 1961; Mayr, 1963; see also,
Claridge et al., 1997; Lherminer and
Solignac, 2000) and are diagnostically
different (Cracraft, 1983). Among primates, closely related species usually
exhibit frequency differences in specific characters, and/or differences in
absolute size and proportions of
structures, or of localized anatomy
(Schultz, 1930, 1936, 1963). The
largely similar phenotypes of closely
related taxa forces systematists to focus on divergent morphology and
magnitude of differences (discontinuities) to define lower taxonomic levels (Simpson, 1961; Mayr, 1963), for
taxa that are not based on objective
criteria (i.e., subspecies, allopatric
species, genus, and to some degree
family). Usually, the greater the magnitude of morphologic differences between closely related taxa, the higher
the corresponding taxonomic category.* Because alpha taxonomy concerns itself with the fundamentals of
identifying species, and species are in
theory the most objective of all taxo-
*To avoid redundancy, the phylogenetic taxonomy of De Queiroz and Gauthier’s (1990, 1992
1994) and De Queiroz’s (1997) does not recognize
categories or levels (i.e., ranks). As such, it is not
utilized to summarize biological differences and
similarities between organisms but is strictly a
system of lineages and evolutionary relationships.
nomic categories (naturally defined by
reproductive communality and phenotypic similarity), alpha taxonomy
imparts some objectivity to all higher
level taxonomy.
With the advent of speciation and associated reproductive isolation, morphologic differences (i.e., discontinuities) greater than those initially
marking the divergence of species accrue with time— either guided by selection or meandering due to drift—
and with the subsequent divergence of
additional species from the ancestral
lineage. Unlike the localized and
quantitative differences distinguishing closely related species, the distinctive (i.e., diagnostic) morphology
characteristic of higher taxonomic
categories may be reflected throughout the organism’s anatomy. It may
involve the appearance of novel anatomical elements (e.g., bones, ligaments, muscles, arteries, and nerves)
and rearrangement of anatomical elements to form new structures.
Categories higher than species are
defined by the divergence of descendant
lineages subsequent to that point in
time when structural innovations are
achieved (Mayr, 1963; McKenna and
Bell, 1997). In this regard, these categories often reflect the success of novel
structures in solving particular physiological or environmental problems and
the subsequent evolutionary radiation
within a lineage that typically follows
such a solution. Large discontinuities
characteristic of the highest taxonomic
levels are correlates of very successful
solutions. In time, the strong competitive edge these solutions afford results
in large discontinuities between a successful lineage and its closest related
outgroup. The number of structural innovations in a lineage and the associated proliferation of descendant lineages, therefore, determine how finely a
higher taxonomic group (i.e., an ancestral lineage and its descendants) may be
divided into hierarchical categories
(Simpson, 1961; Mayr, 1963). Guided
by consistency in a classification, the
taxonomist decides to what taxonomic
level above species any one magnitude
of morphologic difference (or morphologic complexity for categories above
the family level) is assigned.* Because
morphologic changes accrue over generations (a factor of time), increasingly
higher taxonomic levels are distinguished by increasingly greater morphologic discontinuities (Simpson,
1961; Mayr, 1963). The widely divergent phenotypes of species comprising
a higher-level taxon (above family) usually require that higher categories be
based on diagnostic characters (morphologic complexes or qualitative characters). Because morphologic differences between species comprising
higher level taxa may be pervasive
throughout the anatomy, overall quantitative differences are rendered superfluous for classification at higher levels.
Analysis of characters diagnostic of
ascending taxonomic categories within
nested groups at various hierarchical
levels provides insight into how the
characters defining differences in closely
related species are transformed through
time into diagnostic structures or morphologic complexes.
Reconstruction of phylogeny depends
on taxonomy and relies on the morphologic discontinuities that exist among
taxa. Without discontinuities, neither
taxonomy nor phylogeny would be possible. There would be conflation of ancestor and descendant taxa and of the
evolutionary sequence in which characters and structures develop (i.e., polarity). Although direction of evolutionary
change and ancestor-descendant relationships are in part implied by increasing complexity of structure, structural
simplification and/or loss would confound interpretations on the direction
of evolutionary change. Out of necessity, therefore, direction of change and
identification of ancestor-descendant
taxa would be subjective and dependent
on the evaluation of the taxonomist.
The loss of intervening populations and
the morphologic discontinuities that,
*As a rule of thumb, mammalian taxa with (1)
distinctive, quantitative differences throughout
their anatomy are placed in different genera (Gregory, 1910; Robinson, 1962); (2) a unique and distinctive morphologic complex in a localized area
are given the rank of families (Gregory, 1916;
Simpson, 1945; Anderson and Jones, 1984); and (3)
many unique and distinctive morphologic complexes throughout their anatomy are usually
ranked in their own order or class.
over time, result from such a loss permit the reconstruction of phylogeny
and in part the determination of the
direction of evolutionary change. Because the loss of intervening populations does not follow any set pattern,
the taxa existing at any one point in
time are nested within phylogenetic
groups united at different hierarchical
levels, and show varying degrees of relationship and varying degrees of morphologic discontinuity. Nesting of taxa
within groups and designation of outgroups is as central to phylogenetic reconstruction at higher levels as is morphologic discontinuity.
To emphasize relationships as opposed to summarizing degree of differences, phylogenetic reconstructions
are based on shared characters (Tattersall and Eldredge, 1977). Unlike taxonomic categories, phylogenetic groups
are solely defined by the shared characters of its member taxa (Hennig, 1966).
Characters acquired and modified by
descendant taxa after their divergence
from the common ancestor of the
group (autapomorphies) cannot affect
the common phylogenetic history of the
group, no matter how strongly derived
these characters may be. Markedly derived characters, however, may affect
the taxonomic level a group is assigned
to. Regardless, the characters used in
phylogeny, and their identification as
shared characters, ultimately relies on
taxonomic studies distinguishing species and making evident intra- and interspecific character variation.
At intermediate taxonomic levels
(e.g., suborder and family), it may be
uncertain whether characters present
in a phylogenetic group’s crown species
were also present in the groups stem
ancestor and in the earliest members of
each of its crown lineages. At these levels, morphologic discontinuities may be
relatively too great, “shared” characters
too labile, and the number of taxa
and/or hierarchical levels within a
group too few to provide certainty.
With the corresponding decrease in
complexity (i.e., fewer interrelated anatomical elements) of distinctive morphology distinguishing member taxa at
decreasingly lower taxonomic levels,
homoplasies are increasingly more difficult to detect (Gregory, 1934; Sarmiento, 1987; McHenry, 1996; Lockwood and Fleagle, 1999). Divergence of
descendant taxa may be too recent a
phenomenon to enable the evolution of
a complex morphology (Schultz, 1936;
Sarmiento, 1987, 1988, 1998) so that
there is no complexity to leave evidence
of homoplasy (Szalay, 1976; Eldredge
and Cracraft, 1980; Bock, 1981; Szalay
and Bock, 1991). Moreover, closely related taxa are prone to acquiring homoplasies, because they are predisposed by a largely shared phenotype to
arrive at similar solutions when encountering similar problems in the environment. As such, the idea that characters common to all members of a
taxonomic group are homologous is an
assumption, which makes phylogenetic
reconstruction a theoretical endeavor.
As theories, phylogenies are subject to
testing and revision with accumulation
of new data.
To sidestep problems of homoplasies
in phylogenetic reconstruction, cladistic analyses assume all apparent
similarities are homologies and resolve character conflicts by using the
principle of parsimony (Hennig, 1966;
Forey et al., 1992; Schuh, 2000). The
usefulness of cladistic logic lies in its
ability to identify possible homoplasies
among assumed homologies (Hennig,
1966; Kluge, 1983; McHenry, 1996).
Testing of key homologies (i.e., those
which are critical for defining any one
clade), and their rejection as homologies, subsequently leads to alternate
phylogenies and alternate homologies
for further testing. Once identified, possible homologies can be tested through
(1) more rigorous character analyses
comprising character function and underlying anatomical details (Davis, 1964;
Packer and Sarmiento, 1984; Sarmiento,
1987), (2) comparisons of character
lability within closely related groups
at the same taxonomic levels (Mayr,
1963), (3) reconstruction of evolutionary stages pitting structural continuity
of functional complexes against ecological transitions and adaptive shifts.
(Sarmiento, 1995, 1998; Nielsen, 1998),
(4) fossil evidence.
Ultimately, such a process leads to
the most likely phylogeny, one that
assumes a minimum number of homoplasies and assumes them for characters that (1) are labile at the taxonomic levels concerned; (2) show no
clear polarity in member taxa; (3) are
expected to be paralleled or reversed,
given the functional constraints of
evolutionary stages hypothesized for
descendant lineages (Sarmiento, 1987,
1995, 1998; Lockwood and Fleagle,
In cases, where hypothesized homoplasies do not conform to any of
the above criteria, they are still assumed homoplasies if the phylogenetic signal they provide conflicts
with that provided by the majority of
characters. Where there is no overwhelming majority or minority signal
and none of the conflicting characters
or character sets fit “homoplasy criteria,” the phylogeny may not be resolvable.
Cladistic analyses may not be feasible at lower taxonomic levels, with reticular taxa and the resulting lateral
transmission of characters. As such,
reconstruction is a
theoretical endeavor. As
theories, phylogenies
are subject to testing
and revision with
accumulation of new
there is a “line of death” or a “threshold of futility” to cladistic studies that
must be determined empirically
(Wheeler and Platnick, 2000).
Taxonomy usually reflects phylogeny
(Simpson, 1961; Mayr, 1963; Tattersall and Eldredge, 1977, McKenna
and Bell, 1997). The characters defining different taxonomic levels within a
group usually define relationships between members in a group. The lower
the taxonomic level shared, the closer
the implied relationship between taxa
(Simpson, 1961; Mayr, 1963). Among
contemporaneous taxa, correspondence
between phylogeny and taxonomy is especially close at higher levels (above
family). At higher levels, groups have a
long life and inclusion in them out of
necessity is based more on specific diagnostic characters than on magnitude
of differences.
However, phylogeny cannot always
reflect taxonomy. On the one hand,
phylogeny spans long periods, but any
one taxonomic designation applies to
a relatively small cross-section of time
(Andersson, 1990). On the other hand,
there does not seem to be a constant
rate of phenotypic, genotypic, or behavioral change between evolving lineages (Simpson, 1961; Mayr, 1963,
1982). In some cases, the distinctiveness acquired by a particular taxon
since the time of its divergence from
its sister taxon may be best summarized by assigning it to an equal or
higher taxonomic level than the one
which unites its sister taxon to other
more distally related taxa (Simpson,
1961; Mayr, 1963). However, a taxonomy that is out of sync with phylogeny
is not the sole provenance of subjective taxonomic categories. New species may occasionally arise from one
of the many subspecies comprising a
species (Jolly, 1993). A higher taxon
composed of taxa more distantly related to each other than those it excludes is termed paraphyletic, as opposed to monophyletic (i.e., a taxon in
concordance with phylogeny). Although at higher levels (above genus) a
paraphyletic taxon is unacceptable, at
lower levels it is inevitable.
When dealing with ancestor descendant relationships through time, correspondence between phylogeny and
taxonomy breaks down (Andersson,
1990; Szalay, 1993). This breakdown
is exemplified in the inherent problems posed by the binomial system,
which at some point must force an
arbitrary change in the generic designation given to a long succession of
species within an evolving lineage
(Fig. 2). It is also illustrated with the
initial divergence of two closely related species each of which goes on to
give rise to a higher-level group. Taxonomically at the time of divergence,
the two stem species must be placed
within the same genus. Phylogenetically, however, these two species belong to different higher-level groups.
This incongruity exists because phylogenetic groups are defined at their
point of origin and are continuous
through time, whereas taxa are defined relative to each other (at the
Figure 2. Schematic diagram of an evolving lineage composed of six species (A, A⬘, A⬘⬘, B,
C, D), illustrating discordance between taxonomy and phylogeny. Where along a descent
continuum new taxa are designated, is subjective. Along time continuum II, taxa designation is especially problematic, because it involves both a specific and a generic change (by
definition taxa A⬘ and B are sister species and must belong to a different genus than A⬘⬘ and
D) between what must ultimately be a parental population and its immediate descendants. Moreover, if both A and C are sister species representing stem ancestors of two
contemporaneous family groups, time continuum III must also accommodate a change in
family designation.
same point in time) and increase in
level (i.e., categories reflecting discontinuities) by quantum leaps.
Fossils may represent either ancestors
of living taxa (i.e., crown taxa) or descendant lineages with no living members that diverged from the stem ancestor of the group before, during, or
after the divergence of crown taxa
(McKenna and Bell, 1997). Fossils are
useful for systematic studies, because
they may bridge the gap between the
morphologic discontinuities presented
by living taxa. Because many of the
variables bearing on systematics are
rarely known for fossils (e.g., complete phenotype, geographic distribution, population variation, behavior,
ecology, development, and genotype),
living taxa out of necessity must form
the backbone of systematic studies.
Classification of fossils always depends on analogies made to living
taxa and is nearly always restricted to
osseous or dental morphology. The
magnitude of morphologic differences and/or types of morphologic
characters that are chosen to define
taxonomic categories for fossils must
always be guided by those differences
that define corresponding taxonomic
categories for living taxa (Simpson,
1961; Mayr, 1963, 1982).
Unique morphologic complexes or
structures (i.e., qualitative characters)
distinctive and diagnostic of high-level
taxa provide unequivocal means for initial classification of fossils.* Composed
of inter-related anatomical elements,
morphologic complexes (e.g., the mammalian middle ear [Romer, 1974; Lombard and Hetherington, 1993] or mammalian atlanto-occipital and atlantoaxial joint [Courant and Marchard,
2000]) are formed through a series of
adaptive stages within an evolving lineage over a relatively long evolutionary
time span (de Beer, 1937; Hanken and
Hall, 1993). As such, it seems unlikely
they can be converged upon or paralleled without leaving evidence in the
anatomy. Likewise, once lost in ancestral lineages, morphologic complexes
*Although not treated here, initial classification
also entails the correct identification of fossilized
anatomy. Occasionally, the nonhomologous anatomy of disparate life forms may superficially resemble one another, leading to absurd phylogenetic and functional conclusions (Boaz, 1980).
are unlikely to reappear in their descendants without leaving evidence of nonhomology.
The more completely represented a
taxon is by fossil remains, the more detailed its morphology, and the more
characters it exhibits, the better the resolution it provides for low-level classification. Enumeration of differences between fossil taxa without reference to
those characters defining taxonomic
levels among their closest living relatives, however, has no basis in systematic studies. Fossil taxa cannot be classified at lower taxonomic levels than
those specified for the living taxa used
to guide their classification. Without
comparisons to properly classified living taxa, it is impossible to discern if the
distinctiveness perceived for fossil taxa
is a factor of population variation; is of
the same magnitude diagnostic of subspecies, species, or generic differences;
or actually corresponds to higher taxonomic levels. Whether a fossil species
has the same level of intraspecific variation as do objectively defined species—
i.e., those defined on the basis of sympatry (Mayr, 1963) —within the same
taxonomic group may never be known.
Nevertheless, assuming fossil species
have a level of variation within the
range observed in their most closely related living species is a conservative estimate that maintains consistency in
the taxonomy.
Considering that, at the lowest levels, taxonomic resolution (i.e., subspecies and species) often depends on a
complete phenotype and on population variation, only exceptional fossil
assemblages with high representation
of specific taxa may provide the data
necessary for low-level classification.
In the majority of cases, however, fossil remains fail to show the complete
individual or the range of population
variation and are, therefore, likely to
underestimate species or subspecies
numbers (Tattersall, 1992, 1993). On
the other hand, the less likely scenario
that fragmentary fossil remains exhibit only the distinctive and diagnostic localized morphology of two
closely related species may conceivably result in the two being classified
as different genera. In this case, the
assumption is made that the unknown
anatomy in its entirety is as distinctive
as the known fragments. The taxa,
therefore, are separated at a higher
taxonomic level.
Fossils representing stem ancestors
or early members of higher phylogenetic lineages may never provide
enough evidence to place them within
their respective higher lineage, or to
exclude those closely related contemporaries outside of those lineages.
This may be the case even if all of
these fossils are nonreticular taxa.
The parallelisms and reversals that
are bound to occur in closely related
taxa further confound the resolution
these fossils provide. Fragmentary
fossils isolated from other taxa by
large time gaps may present at the
time they are unearthed a unique and
distinctive morphology that may very
well set them apart as unique species
or even genera. When remains of
other more complete, closely related
and contemporary fossil taxa are
found, however, the number and type
of characters present in the original
fossil may not allow taxonomic resolution from its fossil contemporaries.
If the more complete, newly found
fossils clearly represent more than
one species, the original fossil taxon,
which was made nondiagnostic by the
new finds, is in effect a nomen nudum.
Use of fossils in phylogenetic reconstruction depends on fossils presenting
the relevant morphology to provide
some degree of taxonomic resolution.
Fossils with uncertain classification
may lead to circular reasoning when
postulating shared derived characters
for taxa. For example, misclassified fossils may be used to determine character
polarity and the shared condition in
early members of a lineage and, based
on this determination, argue for their
inclusion into the taxonomic group corresponding with this lineage. Although
phylogenetic analysis may be possible
when classifying fossil taxa at the highest taxonomic levels, the lower the level
a fossil can be unequivocally classified
at, the lower the level of the taxonomic
group that needs to be analyzed. At
lower taxonomic levels, comparisons
can include a narrower range of living
and fossil taxa, so that estimates as to
where along a lineage phylogenetic
events and homoplasies occur are more
precise. In this regard, phylogenetic
analyses benefit from unequivocal classification of fossils at low taxonomic
levels (family or below). As long as the
fossil is correctly classified even if it presents a single character, it can provide
tests for character polarity, demonstrate parallelisms and reversals, and
provide a minimum date (from the
present with a known age of deposit)
for phylogenetic events within the
group. However, many more characters
may be necessary to correctly classify a
fossil and unravel its phylogenetic relationships.
As is usually the case for taxonomy,
the more complete the remains of fossil
taxa are, the greater the degree of phylogenetic resolution they afford. Because morphologic complexes indicative of intermediate taxonomic levels
(family, superfamily, or infraorder) are
In the majority of cases,
fossil remains fail to
show the complete
individual or the range
of population variation
and are, therefore, likely
to underestimate
species or subspecies
often localized, fossil remains lacking
these complexes may only provide initial taxonomic resolution at higher levels (e.g., order or class). In these cases,
as long as fossils present sufficient diagnostic characters, finer phylogenetic
resolution may be possible through cladistic analyses. Fossils with relatively
few characters, all of which are labile at
low taxonomic levels (i.e., genus, species, and subspecies within the taxonomic group the fossil initially provides
resolution for), may never provide certain phylogenetic resolution. In these
cases, the odds that shared characters
are homoplasies are too high to use
these characters as diagnostic of a
group (Figure 5). Fossils that resist classification except at the highest taxonomic levels also confound phylogenetic resolution. Increasingly higher
taxonomic levels suggest increasingly
longer evolutionary time spans and
higher numbers of intervening and
crown taxa. Both the latter increase the
odds of parallelisms and reversals between and along descendant lineages,
Fossil remains that fail to present
discontinuous characters, and show
only continuous ones, may also defy
phylogenetic resolution. Although
continuous characters may be converted into discontinuous ones by
bracketing angular or metric values, it
is unclear what advantages a cladistic
analysis based exclusively on such
characters has over phenetics (Bookstein, 1994; Sarmiento and Marcus,
2000). Throughout the evolution of a
lineage, parallelisms and reversals
may conceivably occur many times in
continuous characters without leaving evidence in the anatomy.
When dealing with continuous
characters, phenetic studies based on
multivariate analyses may be more
useful than cladistic studies based on
bracketing metric traits (Sarmiento
and Marcus 2000).* These analyses
and the phenetic trees they arrive at,
however, reflect degree of similarity
and may or may not reflect true relationships. Although overall phenotypic similarity equates with shared
taxonomic categories at lower levels,
similarities in localized anatomy may
or may not suggest close relationships. Simple shapes with few metric
or angular variables may be easily
paralleled or converged upon, but parallelisms or convergences become increasingly less likely with increasing
shape complexity.† The similarities
present in most localized areas of the
anatomy in taxa belonging to the
*Morphometrics or shape analysis may provide
some resolution to the problem of using quantitative characters in cladistics. Although no convincing methods have as of yet been proposed, algorithms based on quantitative shape variables may
be used to summarize discontinuities in shapes
between taxa, and these in theory could be successfully implemented in cladistic analysis.
Whereas cladistics arrives at a shared range of
metric values (bracketed values) for a phylogenetic
group and hypothesizes maximum parsimony to
reconstruct the ancestral condition, phenetics arrives at mean distances (D) between measurements
and hypothesizes minimum distance (i.e., maximum parsimony) for the ancestral condition. In
the case of phenetics, minimum mean distances
are free of subjective categories introduced by taxonomists when bracketing continuous characters.
Finally, the crown hominoid elbow
and wrist joints exhibit a unique morphologic complex of interrelated anatomical elements that allow the hand
and radius to rotate nearly 180 degrees around the ulna (Sarmiento,
1985, 1988). As summarized below,
this complex permits the initial classification of hominoid remains.
Wrist and Elbow Joint Complex
Figure 3. Schematic diagram of character transformations during hominoid wrist joint
evolution, emphasizing the ulnocarpal and pisotriquetral joints. Table 1 summarizes characters present in each hominoid wrist type and in a hypothesized ancestral catarrhine.
(NOTE: From top to bottom, the first six colors in the key correspond to columns numbered
1– 6 in Table 1.) The evolutionary order of development hypothesized for the modern
hominoid wrist joint types is based on increasing character complexity and increasing divergence away from the generalized catarrhine condition (Lewis, 1969; Sarmiento, 1985; 1988).
same genus or family suggest that localized similarities in complex shape
must at least show a corresponding
level of relatedness.
As a group, hominoids present both
benefits and drawbacks to classification and phylogenetic reconstruction.
On the negative side, living hominoid
species, with the exception of hylobatids are few in number. Therefore,
the condition in one or two crown
taxa usually makes the difference as to
whether a character is to be considered a parallelism, a primitive reten-
tion or reversion, or shared derived
(Sarmiento, 1988, 1995, 1998). On the
plus side (Figure 5), hominoids are a
modern group. Analogies made to living hominoids are, thus, more likely
to be both relevant and useful. Moreover, hominoids are known from
many fossil taxa (Szalay and Delson,
1979; Hill and Ward, 1988; Bonis et
al., 1990; Begun and Kordos, 1993;
Benefit and McCrossin, 1995; MoyaSola and Kohler, 1996; Ishida and
Pickford, 1997; Ishida et al., 1999; Senut et al., 2001). As such, character
polarity and phylogenetic events reconstructed from living taxa can be
amply tested against fossil evidence.
Figures 3 and 4 and Table 1 summarize
the elbow and wrist joint characters
that are mechanical requisites of forearm rotation and shows the various
character states for the complex and
the most parsimonious transformations among the five hominoid genera.
Excluding orangutans, variation in the
complex within Hylobates, Pan, Gorilla,
and Homo unites these latter genera in
a cline, in order from most primitive to
most derived. The orangutan complex
clearly shares the hominoid condition,
but it is markedly derived in a separate
direction from humans and African
apes, more than likely from a hylobatidlike condition (Sarmiento, 1985, 1988).
There is little doubt that the hominoid
elbow and wrist joint complex is a
shared derived structure, as indicated
by the following: (1) the unique hominoid complex is formed by a large number of inter-related anatomical elements, including some novel elements.
Yet, the complex in all genera corresponds in anatomical detail exhibiting
intrageneric variation that unites the
various hominoid wrist and joint types
in a cline (Lewis, 1969; Sarmiento,
1988). (2) There is a large morphologic
discontinuity between the hylobatid
complex (the least derived among
hominoids) and the corresponding elbow and wrist joint characters of monkeys, indicating several intervening
adaptive stages are necessary to arrive
at the hominoid complex (Lewis, 1969;
Sarmiento, 1985, 1988). (3) The evolutionary sequences suggested by differences in the joint complex within
hominoids agrees with hominoid phylogenies as independently arrived in
countless studies based on other morphologic characters and on biomolecular analysis (see Stewart and Disotell,
1998). (4) The living hominoid genera
practice widely divergent locomotor behaviors with contrasting different upper limb use, but the joint complex is
Figure 4. The hominoid humeroanterobrachial joint compared with that of a generalized catarrhine. Bony characters associated with the
unique hominoid forearm pronation and supination range are emphasized (Sarmiento, 1985; 1988). In addition, hominoids also show soft
tissue correlates of forearm rotation, e.g., short heads of pronator and supinator muscles and annular radioulnar ligament.
common to all hominoids and has been
modified by each to best suit practiced
behaviors (Sarmiento, 1985, 1988). As a
shared derived complex, the hominoid
elbow and wrist joint serves as a diagnostic structure that can be used to
identify hominoids (Sarmiento, 1987,
Considering the loss of intervening
populations, the marked morphologic
discontinuity between hominoid and
Old World monkey wrist-joints indicates that there must have been early
lineages of extinct hominoids, including the stem ancestor of the group
without full development of the hominoid complex. Identification of these
taxa as early hominoids is possible if
they exhibit a complex approaching
the common condition shared by
crown hominoids. However, it is
problematic if the complex is incipi-
ent, as it is expected to be in those
ancestral hominoids recently diverged
from nonhominoid catarrhines. At a
time, when the distinction between
hominoid and nonhominoid catarrhines
is at the species or generic level, diagnoses as to whether a fossil belongs to
the hominoid lineage must depend on
rather complete remains.
Aside from the elbow and wrist joint
complex, crown hominoids share a
suite of characters, associated with
cautious climbing behaviors that as a
set are diagnostic of the group (Sarmiento, 1987, 1988, 1995). However,
not one of these characters individually presents the morphologic complexity to attest to parallelisms or re-
versals. Hence, when occurring in
isolation, they are not diagnostic of
hominoids (Sarmiento, in preparation). In fact, to one degree or another, many of these characters have
been paralleled by other primates and
converged on by other mammals (Sarmiento, 1995). Because many of these
characters are quantitative and unlikely to document reversals, some
hominoids may exhibit very few cautious climbing characters or remnants
of these characters. Without knowledge as to the evolutionary transformations that led to the shared hominoid condition, presence in a fossil of
one or two characters that are either
part of the cautious climbing complex
or part of the elbow and wrist joint
complex cannot be taken as diagnostic of hominoids.
TABLE 1.‡ Systematic characters in the wrist joints of humans, apes, and a generalized catarrhine precursor
1: Carpoantebrachial
2: Pisotriquetral &
3: Distal radioulnar
4: Pisostylotriquetral &
1. Robust ulnostyloid process
with facets on distal and
radial aspect
2. Bulky cuboidal-like
triquetrum with bifaceted
proximal articulation
3. Bifaceted, robust, and
elongated pisiform
4. Reduced wedge-shaped
triquetrum with vestigial
stylotriquetral contact
5. Distal migration and
reduced pisiform with loss
of ulnopisiform contact
6. Circumferential facet on
ulnar styloid for ‘semilunar
7. Short, markedly
abbreviated non-articular
ulnar styloid process
8. Extensive fusion of ulnar
ligaments to each other
and to triquetrum
separating radiocarpal
and pisotriquetral joints
9. Reduced, cylyndricalshaped triquetrum
1. Mild mediolateral curvature
Cartarrhine 2. Triangular ligament variably
articular with ulnar head
3. Mediolaterally narrow
radiolunate facet
1. Concavo-convex
pisotriquetral facet
2. ‘Meniscus’ absent
1. Incipient synovial distal
radioulnar joint
2. Transversely narrow joint
with its curvature
subtending small central
Gibbons &
5. Ulnar shelf of radius excluding
ulnar head from joint
6. Mediolaterally broad
radiolunate facet
7. Tight mediolateral curvature of
ulnar side
3. Diarthroidal
4. Transversely broad joint
(i.e. large semilunar ulnar
head) with its curvature
subtending large central
(5–7 as in Gibbon)
8. Hypertrophied lunate with
mediolateral curvature for
radial facet subtending large
central angle
3. Bifaceted Pisiform articular
with triquetrum and os
4. Separate ‘semilunar
meniscus’ and triangular
5. Triquetrum’s pisiform facet
poorly demarcated
6. Unifaceted pisiform
articular only with
(6 & 7 as in Gibbon)
9. Bifaceted ulnar head for
triangular disc and distal radius
10. Variable triquetral-triangular
disc facet
(3 & 4 as in Gibbon)
(5 & 6 as in Gibbon)
10. Reduced wedge-shaped
triquetrum non-articular
with ulnar styloid
(9 as in Chimpanzee)
11. Mild mediolateral curvature of
ulnar side
12. Triquetrum articular disc facet
(3 & 4 as in Gibbon)
(Same as Gorilla)
(4 & 5 as in Gibbon)
(6 as in Orangutan)
7. Reduced, but
palmodorsaly elongated
8. Pisotriquetral joint
(6 as in Orangutan)
(7 & 8 as in Chimpanzee)
9. Triquetrum’s pisiform facet
well demarcated
10. Fusion of ‘semilunar
meniscus’ and triangular
ligament, forming single
articular disc
(9 & 10 as in Gorilla)
11. Planar pisiform-triquetral
12. Short pisiform
(8 & 9 as in Gibbon)
(10 as in Chimpanzee)
11. Short markedly
abbreviated nonarticular ulnar styloid
process excluded by
articular disc from
proximal carpal joint
(10 as in Chimpanzee)
(11 as in Gorilla)
(3 & 4 as in Gibbon)
(3 & 4 as in Gibbon)
5: Mid-Carpal
6: Os daubentontriquetral
1. Unfused os centrale
2. Proportion of hamate to
capitate forming ball of
3. Large mediolateral
1. Os daubentonii absent
4. Ball of joint formed
largely by head of
5. Tight mediolateral
curvature of ulnar side
6. Trapezium with large
elongated and curved
2. Os daubentonii
articular with ulnar
(5 as in Gibbon)
7. Ball of joint formed
largely by head of
capitate (rarely
8. Triquetrum migrated
distally to midcarpal
9. Lunotriquetral joint
shallow ball and socket
10. Variable hamate
pisiform facet
(5 as in Gibbon)
11. Spiral hamate
triquetral articulation
12. Os centrale fusion
13. Ball of joint formed
mainly by capitate
(11–13 as in Chimpanzee)
14. Mild mediolateral
curvature of ulnar side
3. Os daubentonii absent
(Same as Gorilla)
(4 as in Chimpanzee)
4. Os daubentonii or its
vestige rarely present
(4 as in Chimpanzee)
*For the purpose of coinciding with past works, Lewis’ (1969) term ‘semi-lunar meniscus’, ‘meniscus’ for short, or ‘menisco/meniscal’ in combination are used here. Functionally however, this structure is best referred to as an
anular ligament.
Column numbers correspond to joint colors as described in Figure 3 legend.
There are a large number of morphologic characters known to distinguish
the five hominoid genera and to group
these at higher levels (Keith, 1915,
1934, 1940; Gregory, 1922; WoodJones, 1929; Schultz, 1936, 1968;
Lewis, 1969; Sarmiento; 1987, 1988,
1995, 1998) (Fig. 5). Siamangs and
gibbons form one of these groups (hylobatids) and humans and African
apes the other (hominoids). Although
orangutans appear to share a common evolutionary history with humans and African apes exclusive of
hylobatids (Schultz, 1936; Sarmiento,
1985, 1988, 1998), the morphologic
characters orangutans share with humans and African apes lack the complexity to unequivocally resolve this.
Because humans and African ape taxa
are closely related, as are the various
species of hylobatids, relationships
within either of these two groups are
not always clear. The larger number
of similarities between gorillas and
humans to the exclusion of chimpanzees is as likely a result of shared
derived ancestry as of parallelisms
owing to a terrestrial lifestyle (Sarmiento, 1983, 1985, 1988, 1994, 1998).
Cladistic analyses aimed at resolving
relationships between humans, gorillas, chimpanzees, orangutans, and hylobatids that consider all of the characters presently known to distinguish
each hominoid genera, including biomolecular evidence have yet to be reported on.
Hominoid alpha taxonomy also
needs to be worked out. This is especially the case in great apes where distinctive populations are allopatric and
species differences have been decided
on magnitude of morphologic differences as opposed to objective criteria
(Groves, 1993; Sarmiento and Butynski, 1996; Sarmiento et al., 1996; Sarmiento and Oates, 2000).
An initial dependence on very fragmentary and incomplete fossils, and the tradition in vertebrate paleontology of relying on teeth for classification, is in
part to blame for past misinterpretations of the hominoid fossil evidence.
With only dental remains considered,
hominids and hominoids were initially
diagnosed on characters that are either
primitive for, or labile in catarrhines,
and/or lack the complexity to test for
homoplasies (i.e., thick molar enamel, a
small canine and a nonsectorial p3, and
the 4 cuspid upper and 5 cuspid lower
molars; Gaudry, 1890; Branco, 1898;
Pilgrim, 1910; Schlosser, 1911; Schwalbe,
1915; Gregory, 1916, 1922; EliottSmith, 1924; Abel, 1931; Simons and
Pilbeam, 1965; Szalay and Delson,
1979). Although the corresponding
characters appeared to be diagnostic
for hominids and hominoids when considering only the crown members of sister taxa (i.e., African apes and cercopithecines, respectively), the characters
were never examined in outgroups to
establish polarity (primitive vs. de-
Because humans and
African ape taxa are
closely related, as are
the various species of
hylobatids, relationships
within either of these two
groups are not always
rived), or within member taxa to gauge
their lability at corresponding taxonomic levels. When alleged fossil hominoid skeletal anatomy, became better
known, the number of parallelisms between the two major catarrhine groups
that were required under certain fossil
classifications forced progressive workers to examine outgroups and recognize
the 4 cuspid upper and 5 cuspid lower
molar pattern as primitive for catarrhines, if not anthropoids (Von Koenigswald, 1969; Sarmiento, 1987). Likewise, to avoid an inordinate number of
parallelisms among catarrhines, hominoids, or the human/African ape clade,
it was necessary to recognize thick
enamel, a small canine, and nonsectorial p3 as labile in anthropoids and
likely to develop in parallel in hominoids and early catarrhines. Hallowed
by usage, however, provisional homi-
noid and hominid classifications proposed early on in the infancy of paleoanthropology on the basis of very
fragmentary Eocene, Oligocene, or
Miocene fossils, and on nondiagnostic
characters, are still followed by some
workers, even in the face of very strong
conflicting evidence (Bloch et al., 1997;
McKenna and Bell, 1997).
Underlying fossil misclassifications
are also uninformed preconceptions,
which blinded workers to alternative
scenarios and gave credence to using
solely dental evidence to diagnose
hominoids and hominids. These preconceptions, which can trace their origin to the very beginnings of vertebrate paleontology and human
evolutionary theory, can be summarized in the following practices: (1)
reconstructing whole animals based
on fragmentary fossil remains and attempts to correctly classify such fragmentary fossils at the lowest taxonomic levels (species or subspecies);
(2) assuming characters present in humans are always the most progressive
and derived, and seldom or never represent an ancestral condition (also applies to those characters humans
share with great apes and/or hylobatids); (3) assuming all catarrhines
with a small canine and a nonsectorial
p3 are hominids.
The first of these has an origin in
Cuvier’s (1812) principle of correlation and is based on a creationist philosophy in which organism types are
immutable. The second finds its origin
in Lamarck’s scala naturae (1809) in
which all living organisms are striving
to become human. It underlies many
preconceptions as to character polarity, thus, resulting in misclassification. The third can be traced to Darwin’s Descent of Man (1871) and the
special significance he accorded to canine reduction as one of a constellation of interdependent human characters, including large brain, manual
dexterity, tool use, and bipedalism. Although Darwin never argued that any
one of these characters alone is diagnostic of humans, providing examples
of their independent development in
other animals, their subsequent enthronement in human evolutionary
theory has given them mythic powers
as diagnostic hominid characters. In
this regard, many workers still fail to
realize that (1) many of the early non-
hominid hominoid fossils have small
canines and nonsectorial premolars
(e.g., Oreopithecus, Ouranopithecus,
and Ramapithecus), (2) several nonhominoid anthropoids have independently arrived at canine reduction
(e.g., Brachyteles, Callicebus, and Alouatta), (3) many nonhominoid catarrhine females have reduced canines
(e.g., Rhinopithecus, Papio, Presbytis,
and Pygathrix). All of which indicate
that reduced canines may be ancestral
for hominoids, relatively labile at intermediate taxonomic levels and in themselves not reliable for diagnosing hominid affinities or higher taxonomic
Guided by Cuvier’s principle of correlation and Lamarck’s scala naturae,
Darwin’s musings have been taken to
the extreme by paleoanthropologists
working on alleged fossil hominids. In
this regard, any character present in
modern humans, which can be correlated with bipedalism, tool use, or
some relative brain enlargement, have
also been argued to be diagnostic of
hominids (Hurzeler, 1960; Simons
and Pilbeam, 1965; Leakey, 1968), especially Homo (Mayr, 1950; Leakey et
al., 1964). This is the case regardless
of whether the characters are common to nonhominid primates, ancestral for hominoids, and/or associated
with other behaviors aside from bipedalism (Sarmiento, 1998, 2001; Sar-
Figure 5. Juvenile (a) orangutan, (b) gorilla,
(c) human, (d) pygmy chimpanzee and (e)
common chimpanzee skulls illustrating the
presence or absence of a mastoid notch
and the cranial bone relationships at pterion. Cladograms (i–vii, on right) show minimum number of homoplasies that must be
posited for characters given currently accepted great ape and human phylogeny.
The mastoid notch character shows three
alternative cladograms (v, vi, vii), all equally
parsimonious with the same minimum number of homoplasies. Cranial bone relationships at pterion produce a single most parsimonious cladogram, but each of the other
alternatives (i, ii, iv) have only one additional homoplasy. Due to low sample number (i.e. number of compared taxa) and
high character heterogeneity within sample, both characters fail to provide phylogenetic resolution. Because both characters are too simple to confidently detect
homoplasies and alternate character states
may exist in low frequency within the same
hominoid taxa, they are equivocal for resolving higher-level taxonomy and usually
poor for taxa diagnosis.
miento and Marcus, 2000) or tool use
(Sarmiento, in preparation). Even in
cases where fossil australopithecines
are known from relatively complete
remains, hominid classification has
still relied on a reduced canine, a nonsectorial premolar, thick molar
enamel, and some human-like skeletal
characters allegedly correlated with
modern human bipedality. The possibility these characters, many of which
are quantitative, may be labile in, or
ancestral for, hominoids is rarely
given serious consideration. The presence in an early hominoid (e.g., Oreopithecus; Straus, 1963; Sarmiento,
1987; Kohler and Moya Sola, 1997) of
many of the same alleged bipedal
characters argued to be diagnostic of
hominids suggests that these characters may be primitive for and/or labile
within hominoids.
The Piltdown hoax speaks volumes
for the power of these preconceptions
to misguide hominid classification. At
the time, the human ancestor everyone hoped to find was expected to be
associated with tools, endowed with a
large brain, and have relatively small
canines and human-like premolar
wear patterns. Thus, Piltdown was
popularly embraced as a human ancestor for nearly half a century (Mayr,
1950), withstanding the scrutiny and
suspicions of the most eminent workers (Miller, 1915; Gregory, 1922; Weidenreich, 1943; Weiner et al., 1953;
see also Milner, 1999). Notably, the
initial proposal that Oreopithecus was
a human ancestor never took hold, despite the presence of reduced canines,
bicuspid nonsectorial p3s, and many
of the alleged bipedal characters, i.e.,
strong ischial spine, bowl-shaped pelvis, strong femoral bicondylar angle
and relatively short pubic symphysis
(Sarmiento, 1987; Kohler and Moya
Sola, 1997). Other factors, therefore,
must also play a role in the acceptance
of fossils as ancestors.
One of us (Sarmiento, 1987) has
noted that incomplete and fragmentary fossils are more likely to be popularly embraced as ancestors than are
more complete ones, which divulge
more specific details. Incomplete fossils accommodate everyone’s preconceptions and can be made to support
personal hypotheses or serve individual agendas. In this regard, Kenyapithecus and Rampithecus (Simons,
1972) known at the time only from
dental remains, and exhibiting a
somewhat reduced canine and a nonhoning premolar, were also posited to
be bipedal tool users, and evidence
was found to support these claims
(Leakey, 1968). The economic and
sociopolitical implications of finding
human ancestors, however, are considerable, and acceptance of fossils as
such rests in part with these concerns.
Many of the problems confronting
hominoid fossil systematics deal with
resolution of late Miocene and Pliopleistocene fossils and separation of
those taxa that predate the human/
African ape split from those that are
members or offshoots of each of the
three crown lineages. It is more than
suspicious that on the African continent, currently inhabited by chimpanzees and gorillas, there are no African
ape ancestors, nor offshoots of either
of these lineages, nor taxa ancestral to
the African ape/human clade during
the Plio-pleistocene, only hominids.
Aside from clinging to the same preconceptions and relying on the same
nondiagnostic characters that incorrectly led Eocene, Oligocene, and
Miocene fossils to be classified as
hominids, paleoanthropologists have
also erred in classifying late Miocene
and Plio-pleistocene fossil hominoids
(1) as new and/or separate taxa based
solely on enumeration of differences
between fossils (ignoring intraspecific
variation and the types of characters
and magnitude of difference defining
lower taxonomic levels in living taxa),
(2) without reference to diagnostic
characters that distinguish higher
level taxonomic groupings in living
hominoids, (3) at lower levels than
those specified for the living taxa used
to guide classifications, (4) on too few
supposedly diagnostic characters in
localized areas of the anatomy without examining character lability or
polarity, (5) on fragments that lack
diagnostic morphology for the taxonomic level in question. It is very unlikely, therefore, that African Pliopleistocene “hominid fossils” are
correctly classified.
Phylogenetic analyses based on in-
correct classifications, are unlikely to
be accurate, because relevant outgroups may be excluded from analysis, and intraspecific and inter-specific
variation conflated. Current fossil
hominoid phylogenies, however, are
also hampered by cladistic analyses
that (1) are made up in large part of
subjectively bracketed continuous
characters; (2) sample too few member taxa and/or no outgroups, so that
hypothesized homoplasies and character polarities are poorly supported;
(3) present initial results as final and
fail to test the likelihood of assumed
homologies and hypothesized homoplasies; (4) use only skull or dental
differences in analyses and ignore diagnostic characters in other areas of
the anatomy, when such evidence is
available; (5) attempt to bridge large
gaps in intervening populations with
characters that are labile at the subspecies and species level; (6) fail to
consider appropriate outgroups given
the taxonomic level of resolution enabled by the fossils.
By no means are these problems the
sole provenance of Late Miocene or
Plio-pleistocene hominoid systematics. These same errors also hamper
systematics of early and middle Miocene catarrhines (Walker et al., 1986;
Gebo et al., 1997; Rae, 1999; Senut et
al., 2000) and hominoids (Ward et al.,
1999) and also cause havoc throughout mammalian systematics. Unlike
other systematists, however, most
hominid paleoanthropologists have
yet to recognize these problems and
make the necessary adjustments.
Lovejoy et al. (1999) suggested that,
within closely related species (i.e., African apes and humans), adult mammalian limb bones can provide important data for phylogenetic or cladistic
analyses if the interplay of local regulating mechanisms (SAMs) and these
authors’ own interpretations of developmental differences in assignment of
positional information (PI) in the
limb bud are considered. Combining
their own interpretations on pelvic
limb development and mechanical
function, they arrive at the following
five character categories: Type 1,
trait(s) that differ in expression, due
to resultant effects of PI on local pattern formation, e.g., hominid ilium
superoinferior length; Type 2, trait(s)
that represent field-derived pleiotropy
and whose morphologic consequences
are selected for (but with no interaction to natural selection processes),
e.g., hominid pubis superoinferior
length; Type 3, trait(s) that differs between taxa due to systemic modifications, e.g., hominid body size; Type 4,
trait(s) that differs in expression between taxa due to interaction of
SAMs, e.g., human femoral bicondylar angle; Type 5, same as Type 4, but
of no diagnostic value, e.g., femoral
anteversion. Lovejoy et al. (1999) suggest these have varying significance in
fossil hominoid systematics and in
functional interpretations.
Unfortunately, the categories proposed by Lovejoy et al. (1999) are
unrealistic and have little heuristic
value for inferring phylogenetic scenarios. It is difficult to envision how,
on the basis of adult mammalian
limb bones (i.e., fossils) alone, one
would be able to interpret differences in PI assignment or claim that
differences in length are the result of
PI. Interspecific differences in adult
limb bone length are also the result
of postembryonic or postnatal differences in rates of cellular expression, morphogen gradients, and hormones, all of which are mediated by
organism interplay with environmental forces. Limb lengths in great
apes can differ without differences
in PI, and this may especially be the
case among closely related taxa (Sarmiento, 1985).
A category composed of limb bone
lengths lacking a mechanical function
as proposed by Lovejoy et al. (1999,
2000) is also unrealistic. It is well
known that skeletal segment lengths
affect the lever arms of muscles or of
adjoining segments and also the moment of inertia of segments, so that
limb bone length affects mechanical
function. The same applies to joint
sets (i.e., femoral bicondylar angle or
femoral anteversions). The claim by
Lovejoy et al. (1999) that the criteria
for assigning characters to each of
their five categories is not actually
necessary, because allocation of extinct organisms into their categories is
hypothetical,* is puzzling. As such, it
is unclear how careful categorization
of characters into their system will
clarify either phylogeny or systematics. Nesting unrealistic hypotheses of
development and function within hypotheses of phylogeny can only result,
at best, in unrealistic speculations.
The recommendation to construct cladograms based on characters that
vary intraspecifically and/or are continuous (i.e., quantitative) to clarify
lower level systematics defies logic
and shows a surprising naiveté and/or
irreverence for modern systematics.
Notably, the majority of current research delimiting developmental mechanisms at the cellular level has been
done on chick embryos. Until similar
research is done on primates and mammals, in a systematic fashion, there is
no way to know (1) the various growth
variable contributions to adult bone
shape; (2) how this contribution varies
with distance of relationship; (3) how
PI simultaneously affects various dimensions of an adult bone.
Nevertheless, it is well known that
in closely related taxa where distinctive body segment proportions are not
developed until adulthood, length differences are more likely the result of
rates of cellular expression as mediated by environmental forces, rather
than of PI (Sarmiento, 1985). Such
hypotheses about differences in PI
among closely related mammalian
taxa, at this point, are not likely to
help unravel human-African ape phylogeny.
If there is any testament to the accuracy
of morphology-based systematics, it is
provided by the recent onslaught of biomolecular studies, which more often
support rather than contradict morphology-based taxonomies and phylogenies. Notably, in those cases where
there are clear contradictions (Graur et
*“How are traits to be allocated to one of these
five categories, given that virtually nothing is
known about their actual genetic basis and that
such knowledge is virtually unobtainable for extinct organisms? Our proposed classification is
not intended to require such knowledge, but only
to encourage observers to formally state the presumed morphogenetic basis of each of the traits
they choose to include in a functional or phyletic
analysis” (Lovejoy et al., 1999 p. 13,251).
al., 1991; Milinkovitch, et al., 1993; Garner and Ryder, 1996), the biomolecular
evidence presented has been shown to
be unreliable for reconstructing phylogeny (Luckett and Hartenberger, 1997;
Philippe, 1997; Naylor and Brown,
1998; Seaman, 2000). Mammalian taxonomy as based on morphology, has
thus remained more or less unchanged.
Progressive workers, therefore, argue
for biomolecular and morphologic
character integration within simultaneous analyses striving for “total evidence” (Kluge, 1989; Nixon and Carpenter, 1997).
However, the systematic interest
molecular studies have generated has
shown that many currently accepted
phylogenies and classifications have
very little molecular or anatomical
data supporting them (Nielsen, 1998).
The need to gather these data to construct well-supported phylogenies and
classifications, especially as pertains
to hominoids and hominids, is fertile
ground for anatomical studies. Regardless of the anatomical subdiscipline (development, histology, gross
anatomy, etc.) these data originate
from, they must adhere to systematic
methodology to be applicable. Hopefully, the future revolution in hominoid and hominid systematics that is
sure to occur will not cause additional
loss of confidence in morphologybased methods but will inspire anatomists to make significant contributions. The reason for this change will
certainly not be founded in the inaccuracy of MBS, but on the long history of preconceptions and the sociopolitical and moral baggage that
comes with unraveling our own history. The latter is the challenge that
makes hominoids such an enjoyable
group to work with.
Abel O. 1931. Die Stellung des Menschen
im Rahmen de Wirbeltiere, Fischer,
Anderson S, Jones JK. 1984. Orders and
families of recent mammals of the
world. New York: Wiley.
Andersson L. 1990. The driving force: species concepts and ecology. Taxon
Begun DR. 1992. Miocene fossil hominids
and the chimp-human clade. Science
257:1929 –1933.
Begun DR, Kordos L. 1993. Revision of
Dryopithecus brancoi SCHLOSSER, 1901
based on the fossil hominoid material
from Rudabanya. J Hum Evol 25:271–285.
Benefit BR, McCrossin ML. 1995. Miocene
hominoids and hominid origins. Annu
Rev Anthropol 24:237–256.
Bloch JI, Fisher DC, Gingerich PD, Gunnel
GF, Simons EL, Uhen MD. 1997. Cladistic analysis and anthropoid origins. Science 278:2134 –2136.
Boaz NT. 1988. Status of Australopithecus
afarensis. Yearb Phys Anthropol 31:85–
Bock WJ. 1981. Functional-adaptive analysis in evolutionary classification. Am
Zool 21:5–20.
Bookstein FL. 1994. Can biometrical shape
be a homologous structure? In: Hall BK,
editor. Homology: the hierarchical basis
of comparative biology. New York: Academic Press. p 198 –229.
Branco W. 1898. Die menschenaähnilichen
Zähne aus dem Bohnerz der Schwäbischen
Alp., Jh. Ver. Vaterl. Naturkde, Württemberg, Teil I, 54:1–144.
Chaline J. 1999. A new view of hominid
evolution. In: Reumer JWF, De Vos J,
editors. Elephants have a snorkel! Papers in honor of Paul Sondaar. Deinsea
7:67– 82.
Chamberlain AT, Wood BA. 1987. Early
hominid phylogeny. J Hum Evol 16:119 –
Claridge MF, Dawah HA, Wilson MR.
1997. Practical approaches to species
concepts for living organisms. In: Claridge MF, Dawah HA, Wilson MR, editors. Species. The units of diversity. London: Chapman and Hall. p 1–16.
Collard M, Wood B. 2000. How reliable are
human phylogenetic hypotheses? Proc
Natl Acad Sci U S A 97:5003–5006.
Conroy GC, Pickford M, Senut B, Van Couvering J, Mein P. 1992. Otavapithecus
namibiensis, first Miocene hominoid
from southern Africa. Nature 356:144 –
Courant F, Marchard D. 2000. Le supraoccipital des Cétés et des Rongeurs foissers. Une convergence morphologique
induite par le pôle post-céphalique? C R
Acad Sci Ser III Sci Vie 323:203–213.
Cracraft J. 1983. Species concepts and speciation analysis. Curr Ornithol 1:159 –
Cuvier G. 1812. Recherches sur les Ossements fossiles de Quadrupeds. Paris.
Darwin C. 1859. On the origins of species
by means of natural selection, or the
preservation of favoured races in the
struggle for life. London: John Murray.
Darwin C. 1871. The descent of man and
selection in relation to sex. London:
John Murray.
Davis DD. 1964. The giant panda. A morphologic study of evolutionary mechanisms. Fieldiana Zoological Memoirs
Chicago: Chicago Natural History Museum.
de Beer GR. 1937. The development of vertebrate skull. London: Oxford University
de Bonis L, de Bouvrain G, Geraads DM,
Koufos G, 1990. New hominoid skull
material from the late Miocene of Macedonia in Northern Greece. Nature 345:
De Queiroz K. 1997. The Linnean hierarchy and the evolutionization of taxonomy, with emphasis on the problem of
nomenclature. Aliso 15:125–144.
De Queiroz K, Gauthier J. 1990. Phylogeny
as a central principle in taxonomy: phylogenetic definitions of taxon names.
Syst Biol 39:307–322.
De Queiroz K, Gauthier J. 1992. Phylogenetic taxonomy. Annu Rev Ecol Syst 23:
449 – 480.
De Queiroz K, Gauthier J. 1994. Toward a
phylogenetic system of biological nomenclature. Trends Ecol Evol 9:27–31.
Eldredge N, Cracraft J. 1980. Phylogenetic
patterns and evolutionary process:
method and theory in comparative biology. New York: Columbia University
Eliott-Smith G. 1924. Essays on the evolution of man. Oxford: Oxford University
Eliott-Smith G. 1925. The fossil anthropoid ape from Taung. Nature 115:236.
Foley R. 2001. In the shadow of the modern synthesis? Alternative perspectives
on the last fifty years of paleoanthropology. Evol Anthropol 10:5–14.
Forey PL, Humphries CJ, Kitching IL,
Scotland RW, Siebert DJ, Williams DM.
1992. Cladistics: a practical course in
systematics. Oxford: Clarendon Press.
Franciscus RG. 1999. Neanderthal nasal
structures and upper respiratory tract
“specialization.” Proc Natl Acad Sci U S A
Garner KJ, Ryder OA. 1996. Mitochondrial
DNA diversity in gorillas. Mol Phylogenet Evol 6:39 – 48.
Gaudry A. 1890. Le dryopithèque, Mem.
Soc. Geol. France, Pal. Mem. 1:1–11.
Gebo DL, MacLatchy L, Kityo R, Deino A,
Kingston J, Pilbeam D. 1997. A hominoid genus from the early Miocene
Uganda. Science 276:401– 404.
Gingerich PD. 1973. Anatomy of the temporal bone in the Oligocene anthropoid
Apidium and the origin of Anthropoidea.
Folia Primatol 19:329 –337.
Graur D, Hilde WA, Li WH. 1991. Is the
guinea pig a rodent? Nature 351:649 –
Gregory WK. 1910. The orders of mammals Bull Am Mus Nat Hist 27:1–524.
Gregory WK. 1916. Studies on the evolution of primates. Bull Am Mus Nat Hist
35:239 –355.
Gregory WK. 1922. The origin and evolution of the human dentition. Baltimore:
Williams and Wilkins.
Gregory WK. 1934. Man’s place among the
anthropoids. Oxford: Clarendon Press.
Groves CP. 1993. Speciation in living hominoid primates. In: Kimbel WH, Martin
LB, editors. Species, species concepts,
and primate evolution.. New York and
London: Plenum Press. p 109 –122.
Hall BK. 1994. Homology: the hierarchical
basis of comparative biology. New York:
Academic Press.
Hanken J, Hall BK. 1993. The skull. Vol. 1,
Development; Vol. 2, Patterns of structural and systematic diversity; Vol. 3,
Functional and evolutionary mechanisms, Chicago and London: Chicago
University Press.
Hennig W. 1966. Phylogenetic systematics.
Urbana: University of Illinois Press.
Hill A and Ward S. 1998. Origin of the
hominidae: the record of African large
hominoid evolution between 14 my and
4 my. Yrbk Phys Anthropol 31:49 – 83.
Howells WW. 1973. Cranial variation in
man: a study by multivariate analysis.
Peabody Museum Papers 67:1–259.
Howells WW. 1989. Skull shapes and the
map: craniometric analyses in the dispersion of modern Homo. Papers in the
Peabody Museum of Archaeology and
Ethnology, Harvard University 79:1–189.
Hurzeler J. 1960. The significance of Oreopithecus in the genealogy of man. Triangle 4:164 –174.
Huxley TH. 1895. On the origin of species.
New York: Appleton and Co.
Ishida H, Pickford M. 1997. A new late
Miocene hominoid from Kenya: Samburupithecus kiptalami gen. et sp. nov. C R
Acad Sci Earth Planetary Sci 325:823–
Ishida H, Kunimatsu Y, Nakatsukasa M,
Nakano Y. 1999. New hominoid genus
from the Middle Miocene of Nachola,
Kenya. Anthropol Sci 107:189 –191.
Jolly CJ. 1993. Species, subspecies, and baboon systematics. In: Kimbel WH, Martin LB, editors. Species, species concepts, and primate evolution. New York
and London: Plenum Press. p 67–108.
Kappelman J, Simons EL, Swishe CC.
1992. New age determinations for the
Eocene-Oligocene boundary sediments
in the Fayum depression, Northern
Egypt. J Geol 100:647– 688.
Keith A. 1915. The antiquity of man. London: William and Norgate.
Keith A. 1925. The fossil anthropoid ape
from Taungs. Nature 115:234 –235.
Keith A. 1934. The construction of man’s
family tree. London: Watts.
Keith A. 1940. Fifty years ago. Am J Phys
Anthropol 26:251–267.
Kluge AG. 1983. Cladistics and the classification of the great apes. In: Ciochon
RL, Corruccini RS, editors. New interpretations of ape and human ancestry.
New York and London: Plenum Press. p
180 –220.
Kluge AG. 1989. A concern for evidence
and a phylogenetic hypothesis of relationships among Epicoates (Boidae, Serpentes). Syst Zool 38:7–25.
Kohler M, Moya Sola SJ. 1997. Ape-like or
hominid-like? The positional behavior of
Oreopithecus bambolii reconsidered.
Proc Natl Acad Sci U S A 94:11747–
Lamarck JB. 1809. Zoological philosophy.
Chicago: University of Chicago Press.
Larson SG. 1998. Parallel evolution in the
hominoid trunk and forelimb. Evol Anthropol 6:87–99.
Le Gros Clark WE. 1950a. Hominid characters of the australopithecine dentition.
J R Anthropol Inst 80:37–54.
Le Gros Clark WE. 1950b. New paleontological evidence bearing on the evolution
of hominoidea. Q J Geol Soc Lond 105:
224 –264.
Le Gros Clark WE. 1955. The os inominatum of the recent Pongidae with special
reference to that of the Australopithecinae. Am J Phys Anthropol 13:19 –27.
Leakey LSB. 1967. An early Miocene member of Hominidae. Nature 213:155–163.
Leakey LSB. 1968. Bone smashing by late
Miocene Hominidae. Nature 218:528 –
Leakey LSB, Tobias PV, Napier J. 1964. A
new species of the genus Homo from
Olduvai Gorge. Nature 202:7–10.
Lewis OJ. 1969. The hominoid wrist joint.
Am J Phys Anthropol 30:251–285.
Lherminer P, Solignac M. 2000. L’espèce:
définitions d’auteurs. C R Acad Sci Ser
III Sci Vie 323:153–165.
Lieberman DE. 1995. Testing hypotheses
about recent human evolution from
skulls: integrating morphology, function, development, and phylogeny. Curr
Anthropol 36:159 –196.
Lieberman DE. 1999. Homology and hominid phylogeny: problems and potential
solutions. Evol Anthropol 7:142–151.
Lieberman DE, Pilbeam DR, Wood B.
1996. Homoplasy and early Homo: an
analysis of the evolutionary relationships of H. habilis sensus stricto and H.
rudolfensis. J Hum Evol 30:97–120.
Lockwood CA, Fleagle JG. 1999. The recognition and evaluation of homoplasy in
primates and human evolution. Yearb
Phys Anthropol 42:189 –232.
Lombard RE, Hetherington TE. 1993.
Structural basis of hearing and sound
transmission. In: Hanken J, Hall BK, editors. The skull: functional and evolutionary mechanisms. Vol. 3. Chicago and
London: Chicago University Press. p
Lovejoy CO, Cohn MJ, White TD. 1999.
Morphologic analysis of mammalian
limbs: a developmental perspective. Proc
Natl Acad Sci U S A 96:13247–13252.
Lovejoy CO, Cohn MJ, White TD. 2000.
The evolution of mammalian morphology: a developmental perspective. In:
O’Higgins P, Cohn MJ, editors. Development growth and evolution. London:
Linnean Society. p 41–55.
Luckett WP, Hartenberger JL. 1997. Monophyly or polyphyly of the order Rodentia: possible conflict between morphological and molecular interpretations. J
Mamm Evol 1:127–147.
Mayr E. 1950. Taxonomic categories in
fossil hominids. Cold Spring Harbor
Symp Quant Biol 15:109 –118.
Mayr E. 1963. Populations, species, and
evolution. Massachusetts: Harvard University Press.
Mayr E. 1982. The growth of evolutionary
thought. Cambridge: Harvard University
McCollum MA. 1999. The robust australopithecine face: a morphogenetic perspective. Science 284:301–305.
McCollum MA. 2000. Subnasal morphological variation in fossil hominids: a reassessment based on new observations
and recent developmental findings. Am J
Phys Anthropol 112:275–283.
McHenry HM. 1996. Homoplasy, clades
and hominid phylogeny. In: Meikle WE,
Howell FC, Jablonski NG, editors. Contemporary issues in human evolution.
San Francisco: California Academy of
Science. p 77–91.
McKenna M, Bell SK. 1997. Classification
of mammals above the species level.
New York: Columbia University Press.
Milinkovitch MC, Orti G, Meyers A. 1993.
Revised phylogeny of whales suggested
by mitochondrial ribosomal DNA sequences. Nature 361:346 –348.
Miller GS. 1915. The jaw of Piltdown man.
Smithson Misc Collect 65:1–31.
Milner R. 1999. Huxley’s bulldog: The battles of E. Ray Lankester (1846 –1929).
Anat Rec (New Anat) 257:90 –95.
Moya-Sola S, Kohler M. 1996. A Dryopithecus skeleton and the origins of great ape
locomotion. Nature 379:156 –159.
Naylor GJP, Brown WM. 1998. Amphioxus
mitochondrial DNA, chordate phylogeny, and the limits of inference based on
comparisons and sequences. Syst Biol
Nielsen C. 1998. Morphologic approaches
to phylogeny. Am Zool 38:942–952.
Nixon KC, Carpenter JM. 1996. On simultaneous analysis. Cladistics 12:221–241.
Oakely KP. 1952. Swanscombe Man. Proc
Geol Assoc 63:271–300.
Oakley KP. 1954. Dating of the Australopithecinae of Africa. Am J Phys Anthropol 12:9 –23.
Oakley KP, Hoskins CR. 1950. New evidence of the antiquity of Piltdown Man.
Nature 165:379.
Olson T. 1985. Cranial morphology and
systematics of the Hadar fossil hominids
and A. africanus. In: Delson E, editor.
Ancestors: the hard evidence. New York:
Alan R. Liss. p 102–119.
Osborn HF. 1922. Men of the old stone age,
their environment, life and art. 3rd ed.
New York: Charles Scribner and Sons.
Packer D, Sarmiento EE. 1984. External
and middle ear characteristics of primates, with reference to tarsier-anthropoid affinities. Am Mus Novit 2787:1–23.
Phillipe H. 1997. Rodent monophyly: pitfalls of molecular phylogenetics. J Mol
Evol 45:712–715.
Pilbeam DR. 1967. Man’s earliest ancestors. Sci J 3:47–53.
Pilbeam DR. 1968. The earliest hominids.
Nature 219:1335–1338.
Pilbeam DR. 1969. Newly recognized mandible of Ramapithecus. Nature 222:1093.
Pilbeam DR. 1970. Gigantopithecus and
the origins of Hominidae. Nature 225:
Pilbeam DR. 1972. The ascent of man. New
York: Macmillan.
Pilbeam DR. 2000. Hominoid systematics:
the soft evidence. Proc Natl Acad Sci
U S A 97:10684 –10686.
Pilbeam DR, Rose MD, Barry JC, Shah I.
1990. New Sivapithecus humeri from Pakistan and the relationship of Sivapithecus and Pongo. Nature 348:237–239.
Pilgrim GE. 1910. Notices of mammalian
genera and species from the Tertiaries of
India. Rec Geol Surv India 40:63–71.
Rae T. 1999. The maxillary sinus in primate paleontology and systematics. In:
Koppe T, Nagai H, Alt K, editors. The
paranasal sinuses of higher primates: development, function, and evolution. Berlin: Quintessenz. p 177–189.
Robinson JT. 1954. The genera and species
of the Australopithecinae. Am J Phys Anthropol 12:181–200.
Robinson JT. 1962. The origin and adaptive radiation of the australopithecines.
In: Kurth G, editor. Evolution and hominization. Stuttgart: Gustav Fischer Verlag. p 120 –140.
Robinson JT. 1965. Homo habilis and the
australopithecines. Nature 205:121–124.
Romer A. 1974. Vertebrate paleontology.
Chicago: University of Chicago Press.
Ruvollo M, Disotell TR, Allard MW, Brown
WM, Honeycutt RL. 1991. Resolution of
the African hominoid trichotomy by use
of a mitochondrial gene sequence. Proc
Natl Acad Sci U S A 88:1570 –1574.
Ruvollo M, Zehr S, Pan D, von Dornum M,
Chang B, Lin J. 1993. Mitochondrial
COII sequences and modern human origins. Mol Biol Evol 10:1115–1135.
Ruvollo M, Pan D, Zehr S, Goldberg T,
Disotell TR, von Dornum M. 1994. Gene
trees and hominoid phylogeny. Proc Natl
Acad Sci U S A 91:8900 – 8904.
Sarmiento EE. 1983. The significance of
the heel process in anthropoids. Int J
Primatol 4:127–152.
Sarmiento EE. 1985. Functional differences in the skeleton of wild and captive
orangutans and their adaptive significance. PhD dissertation. New York University, New York.
Sarmiento EE. 1987. The phylogenetic position of Oreopithecus and its significance in the origins of the Hominoidea.
Am Mus Novit 2881:1– 44.
Sarmiento EE. 1988. Anatomy of the hominoid wrist joints, its evolutionary and
functional implications. Int J Primatol
Sarmiento EE. 1994. Terrestrial traits in
the hands and feet of gorillas. Am Mus
Novit 3009:1–56.
Sarmiento EE. 1995. Cautious climbing
and folivory: a model of hominoid differentiation. Hum Evol 10:289 –321.
Sarmiento EE. 1998. Committed bipeds
generalized quadrupeds and the shift to
open habitats: an evolutionary model of
hominid divergence. Am Mus Novit
Sarmiento EE. 2001. Letter to the Editor.
Evol Anthropol 10:15.
Sarmiento EE, Butynski TM, Kalina J.
1996. Gorillas of Bwindi-impenetrable
forest and the Virunga volcanoes: taxo-
nomic implications of morphological
and ecological differences. Am J Primatol 40:1–21.
Sarmiento EE, Butynski TM. 1996. Present
problems in gorilla taxonomy. Gorilla J
Sarmiento EE, Marcus LF. 2000. The os
navicular of humans, great apes, OH 8,
Hadar, and Oreopithecus: functions,
phylogeny, and multivariate analyses.
Am Mus Novit 3288:1–38.
Sarmiento EE, Oates JF. 2000. The Cross
River Gorillas: a distinct subspecies Gorilla gorilla diehli Matschie. Am Mus Novit 3305.
Schlosser M. 1911. Beträge zur Kenntnis
der oligozanen Landsäugetiere aus dem
Fayum, Ägypten, Beitr. Pal. OesterreichUngarns und Orients 24:51–167.
Schlosser M, von Zittel KA. 1923. Grundzüge der Paläontologie. 4 Aufl. München
and Berlin: Oldenbourg.
Schuh RT. 2000. Biological systematics:
principles and applications. Ithaca and
London: Cornell University Press.
Schultz AH. 1930. The skeleton of the
trunks and limbs of higher primates.
Hum Biol 2:303– 438.
Schultz AH. 1936. Characters common to
higher primates and characters specific
to man. Q Rev Biol 11:259 –283, 425–
Schultz AH. 1963. Age changes, sex differences, and variability as factors in the
classification of primates. In: Washburn
SL, editor. Classification and human
evolution. Chicago: Aldine. p 85–115.
Schultz AH. 1968. The recent hominoid
primates. In: Washburn SL, Jay PC, editors. Perspectives on human evolution.
New York: Holt, Rinehart and Winston.
p 122–195.
Schwalbe G. 1915. über den fossilen Affen
Oreopithecus bambolii. Z Morphol Anthropol 19:149 –254.
Seaman MIJ. 2000. Evolutionary genetics
of gorillas. PhD thesis, Yale University.
Senut B, Pickford M, Gommery D, Kunimatsu
Y. 2000. Un nouveau genre d’hominoide du
Miocene inferieur d’Afrique orientale: Ugandapithecus major (Le Gros Clark and
Leakey, 1950) C R Acad Sci Tierre Plantes
Senut B, Pickford M, Gommery D, Mein P,
Cheboi K, Coppens Y. 2001. First hominoid from the Miocene (Lukeino formation, Kenya) C R Acad Sci Earth Planetary Sci 322:137–144.
Simons EL. 1963. Some fallacies in the
study of hominid phylogeny. Proc Int
Congr Zool 4:25–70.
Simons EL. 1965. New fossil apes from
Egypt and the initial differentiation of
Hominoidea. Nature 205:135–139.
Simons EL. 1967. The earliest apes. Sci Am
217:28 –35.
Simons EL. 1972. Primate evolution: an
introduction to man’s place in nature.
New York: Macmillan.
Simons EL, Pilbeam DR. 1965. Preliminary revision of the Dryopithecinae
(Pongidae, Anthropoidea). Folia Primatol 3:81–152.
Simpson GG. 1945. The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85:1–350.
Simpson GG. 1961. Principles of animal
taxonomy. New York: Columbia University Press.
Simpson GG. 1963. The meaning of taxonomic statements. In: Washburn SL, editor. Classification and human evolution.
Chicago: Aldine. p 1–31.
Stewart CB, Disotell T. 1998. Primate evolution: in and out of Africa. Curr Biol
Straus WL. 1963. The classification of
Oreopithecus. In: Washburn SL, editor.
Classification and human evolution. Chicago: Aldine. p 146 –177.
Szalay FS. 1976. Systematics of the omoyidae (Tarsiifomes, Primates): taxonomy,
phylogeny, and adaptations. Bull Am
Mus Nat Hist 156:157– 450.
Szalay FS. 1993. Species concepts: the
tested, the untested, and the redundant.
In: Kimbel WH, Martin LB, editors. Species, species concepts, and primate evolution. New York and London: Plenum
Press. p 21– 42.
Szalay FS, Bock WJ. 1991. Evolutionary
theory and systematics: relationships between process and patterns. Z Zool Syst
Evolutionsforsch 29:1–39.
Szalay FS, Delson E. 1979. Evolutionary
history of the primates. New York: Academic Press.
Tattersall I. 1992. Species concepts and
species identification in human evolution. J Hum Evol 22:341–349.
Tattersall I. 1993. Speciation and morphological differentiation in the genus Lemur. In: Kimbel WH, Martin LB, editors.
Species, species concepts, and primate
evolution. New York and London: Plenum Press. p 163–176.
Tattersall I, Eldredge N. 1977. Fact, theory
and fantasy in human paleontology. Am
Sci 65:204 –211.
Van Couvering JA, Harris JM. 1993. Late
Eocene age of the Fayum mammal faunas. J Hum Evol 21:241–246.
Virchow R. 1895. Weiter Mittheilungen
über den Pithecanthropus erectus Dub.
Verh Dtsch Ges Anthropol Zeit Ethnol
XXVII:648 – 656.
Von Koenigswald GHR. 1956. Gebissreste
von Menschenaffen aus dem unterplio-
zoan Rheinhessens Kon. Ned Akad
Wetensch Amst Ser B 59:318 –384.
Von Koenigswald GHR. 1969. Miocene
Cercopitehcoidea and Oreopithecoidea
from the Miocene of East Africa. In:
Leaky LSB, editor. Fossil Vertebrates of
Africa. London: Academic Press. 1:39 –
Vrba ES, Denton GW, Partridge TC,
Buckle LH. 1995. Paleoclimate and evolution, with emphasis on human origins.
New Haven and London: Yale University
Walker AC. 1969. Fossil mammal locality
on Mount Elgon, Eastern Uganda. Nature 223:591–596.
Walker AC, Rose MD. 1968. Some hominoid vertebra e from the Miocene of
Uganda. Nature 217:980 –981.
Walker AC, Teaford MF, Leakey RE. 1986.
New information concerning the R114
Proconsul site, Rusinga Island, Kenya.
In: Else JG, Lee PC, editors. Primate evolution. Cambridge: Cambridge University Press. p 144 –149.
Ward S, Brown B, Hill A, Kelley J, Downs
W. 1999. Equatorius: a new hominoid
genus from the middle Miocene of Kenya. Science 285:1382–1386.
Weidenreich F. 1943. The skull of Sinanthropus Pekinensis; A comparative study
on a primitive Hominid skull. Palaeontologia Sinica 127: New series 10. p. 485.
Weiner JS. 1955. The Piltdown forgery. Oxford: Oxford University Press.
Weiner JS, Oakley KP, Le Gros Clark WE.
1953. The solution of the Piltdown problem. Bull Bri Mus Nat Hist Geol 2:139 –
Wheeler QD, Platnick N. 2000. The phylogenetic species concept. In: Wheeler QD,
Meier R, editors. Species concepts and
phylogenetic theory. New York: Columbia University Press. p 55– 69.
White TD, Suwa G, Asfaw B. 1994. Australopithecus ramidus, a new species of
early hominid from Aramis, Ethiopia.
Nature 371:306 –312.
Wood B, Collard M. 1999. The human genus. Science 284:65–71.
Woodward A. 1917. Fourth note on the
Piltdown gravel, with evidence of a second skull of Eoanthropus dawsoni. Q J
Geol Soc Lond 73:1–10.
Woodward A. 1925. The fossil anthropoid
ape from Taungs. Nature 115:235–236.
Wood-Jones F. 1929. Man’s place among
the mammals. New York: Longman’s
Green and Co.
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base, systematic, morphology, problems, hominoid, mbs, fossil, hominis
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