Adaptive explanation for the origins of the anthropoidea (primates)

Transcription

American Journal of Primatology 40205-230 (1996)
RESEARCH ARTICLES
Adaptive Explanation for the Origins of the
Anthropoidea (Primates)
CALLUM ROSS
Department of Anatomical Sciences, State University of New York at Stony Brook,Stony
Brook, New York
A new explanation for the origin of the primate suborder Anthropoidea is
presented. Functional analyses of the "forward"-facing orbits, postorbital
septum and retinal fovea are used to reconstruct the morphological and
ecological contexts in which these features are most likely to have evolved.
The postorbital septum is argued to have evolved as an adaptation to
protect the orbital contents from encroaching fibers of anterior temporalis.
This encroachment resulted from increasing convergence and frontation of
the orbital margins in a lineage of small-bodied animals with relatively
large eyes. Increasing orbital convergence is hypothesized to have resulted
from reduction in relative orbit diameter associated with a shift to diurnality at small body size (<1,300g). Increased frontation (verticality) of
the orbital margins is hypothesized to have been due to rostra1 displacement of the superior orbital margin or increasing basicranial flexion in a
lineage of animals with orbits pushed to the midline below the olfactory
tract. Either of these changes would have occurred as a result of increases
in neocortex size. Increased neocortical volume is hypothesized to have
resulted from a shift to group living associated with a shift to diurnality.
Diurnal, visual predation among other vertebrates is commonly associated
with possession of a retinal fovea and the haplorhine fovea is hypothesized
to have evolved in a similar context. All these features are hypothesized to
have evolved in association with a shift from nocturnal to diurnal visual
predation of insects a t small body size and this adaptive shift is argued to
be the defining feature of the anthropoid suborder. The omomyid skull is
the best structural antecedent of the anthropoid skull; however, if basal
primates exhibited moderate degrees of orbital convergence and frontation, orbits that were closely approximated below the olfactory tract and
nocturnal habits, they could easily have given rise to the anthropoid stem
species. The presence of a retinal fovea and lack of a tapetum lucidum in
extant tarsiers implies that they shared a diurnal ancestry with anthropoids. This suggests that the adaptive explanation for anthropoid origins
presented here applies to the origins of the haplorhine stem lineage.
0 1996 Wiley-Liss, Inc.
Received October 2, 1995; revision accepted June 11, 1996.
Address reprint requests to Callum Ross, Anatomical Sciences, S.U.N.Y. at Stony Brook, Stony Brook,
NY 11794-8081.
0 1996 Wiley-Liss, Inc.
206 / Ross
INTRODUCTION
Monkeys, apes and humans constitute a morphologically diverse radiation of
mammals sharing a distinctive complex of morphological features such as a postorbital septum formed predominantly by the zygomatic bone, robust vertically
implanted lower incisors and a retinal fovea. Consequently, they have long been
classified together in a single group: Anthropoidea or Simiiformes [e.g., Linnaeus,
1766; Geoffroy & Cuvier, 1795; Geoffroy, 1812; Cuvier, 1817; Mivart, 1864). Despite a rapidly improving fossil record of early anthropoids (Simons, 1989, 1990,
1992,1995; Simons et al., 1994; Godinot & Mahboubi, 1992, 1994; Godinot, 19943
many questions regarding their origins remain unanswered. What were the forces,
selective or otherwise, that caused Anthropoidea to diverge from their prosimian
(nonanthropoid) ancestors? What were the original functions of the features defining Anthropoidea and what functions do they perform now? In terms of more
general issues in evolutionary morphology, were these features “evolutionary innovations” (Nitecki, 1990); i.e., were they causally related to the subsequent evolutionary diversification of anthropoids?
Previous Explanations of Anthropoid Origins
The first explanations for the existence of the distinctive anthropoid features
reduced them to expressions of orthogenetic evolutionary trends pervading the
primate order [Elliot Smith, 1924; Wood Jones, 1917; Clark, 19341. The first adaptive explanations for the origins of anthropoids were presented by Cartmill [1970]
and Cachel [1979a,bl. Working in the milieu of Simpson’s view that the origins of
higher taxa should be traced to significant adaptive shifts [Simpson, 19611, Cartmill and Cachel posited specific selective forces to explain the adaptive shift defining Anthropoidea.
Cartmill’s Hypotheses. Cartmill [19701 posited that anthropoid origins
could be traced to “an as yet unidentified group of prosimians displaying an apical
interorbital septum and corollary anterior displacement of the olfactory fossa, as in
Tarsius or Pseudoloris, [which] began to undergo an adaptive shift to a diurnal and
largely herbivorous way of life . . .” (Cartmill, 1970, p. 411). This shift to diurnality
was claimed to have resulted in a reduction in orbital diameter, allowing the
braincase to expand forward over the orbits, increasing the degree of orbital &ontation (or the “verticality” of the orbital margins), and producing a n animal much
like a small platyrrhine. Expansion of the anterior portion of the braincase, accompanied by reduction in orbital diameter,
narrowed the gap between braincase and postorbital bar. This encouraged the
spread of periorbital ossification downward from the superior postorbital process (or the expansion of a partial septum of the sort seen in Tarsius) to
insulate the eyeball, with its increasingly fine-grained diurnal retina, from
impulses originating in the muscular and osseous masticatory apparatus filling the temporal fossa [Cartmill, 1970, p. 4121.
Thus, Cartmill explained increased frontation or verticality of the orbits, expansion of the neurocranium out over the orbits and the origins of the postorbital
septum, as the logical consequences of a shift to diurnality and reduction in relative orbit diameter in a lineage of tarsier-like forms. Under Cartmill’s scheme,
possession of a postorbital septum in a tarsier-like animal was a prerequisite for
the evolution of a retinal fovea: without a postorbital septum, Cartmill implied, the
orbital contents are not well enough insulated to allow the evolution of a fovea.
One problem with linking the evolution of a postorbital septum to the presence
Anthropoid Origins I 207
of a fovea in a lineage of tarsier-like animals is that foveae are rare in nocturnal
animals, and extremely rare in animals, like Tursius, that exhibit a retina consisting only of rods [Walls, 19421. If the septum did evolve to insulate a foveate
retina, it is unlikely to have done so in a lineage of nocturnal animals like Tursius.
This problem led Cartmill to propose a different hypothesis for the evolution of the
distinctive anthropoid cranial features [Cartmill, 19801. The absence of a tapetum
lucidum and the presence of a retinal fovea in Tursius suggested to him that the
stem lineage of tarsiers and anthropoids, in which the postorbital septum and
fovea evolved, consisted of diurnal animals. He suggested that these animals were
Suimiri-like, frugivore-insectivores that visually scanned their environment for
insects while chewing their last piece of food. The fovea and postorbital septum
evolved simultaneously, the septum to insulate the foveate eye against masticatory movements in the temporal fossa. To avoid competition with birds, the lineage
leading to Tursius reverted to a nocturnal lifestyle, resulting in the loss of retinal
cones, and massive ocular hypertrophy to compensate for the lack of a tapetum.
Ocular hypertrophy in turn resulted in increased basicranial flexion, with attendant “spatial-packing problems,” necessitating the spread of the medial pterygoid
muscle through the inferior orbital fissure to take origin from the medial orbital
wall. Unlike tarsiers, the stem lineage of anthropoids managed to maintain a
diurnal lifestyle by evolving a fused mandibular symphysis [Beecher, 19791 and
color vision, allowing them to avoid competition with birds by exploiting a diet of
unripe fruits.
Cachel’s hypothesis. An alternative explanation for the origin of the distinctively anthropoid features was presented by Cachel [1979a,bl. In her scheme,
the origin of anthropoids was the result of increasing global seasonality in the late
Eocene [Cachel, 1979al. Increased seasonality was claimed to make fruit resources
more predictable, making them a viable dietary resource for large-bodied primates. Resurrecting Polyak’s [1957] thesis that color vision evolved in primates to
allow them to find ripe fruit by sight, Cachel suggested that increased body size,
diurnality, and frugivory were all interrelated with the evolution of color vision
[Cachel, 1979a, p. 3561. Emphasis on vision for locating food resources led to the
evolution of neurological features distinctive of anthropoids, such as an increased
size of the neocortex in general, and of the temporal lobe in particular, and in a
reduction in size of the olfactory bulbs.
Cachel [1979bl suggested that fmgivory “or extensive incisal preparation of
food” was also causally related to the evolution of the anthropoid postorbital septum. She suggested that the postorbital septum evolved to facilitate enlargement
of the anterior temporalis muscle by augmenting the area available for its origin.
This additional anterior temporalis improved its ability to contribute to vertically
directed bite forces at the incisors [Cachel, 1979bl. Cachel argued that the postorbital septum in Tursius evolved “in response to mechanical demands for support of
hypertrophied eyes, rather than because of masticatory demands” [Cachel, 1979b,
p. 131.
Rosenberger’s hypothesis. Rosenberger proposed that the anthropoid synapomorphies arose as adaptations “for the harvesting of tough-coated fruits and,
possibly, fruits with hard edible contents, such as seeds and nuts” [Rosenberger,
1986, p. 771. Rosenberger suggested that masticatory forces “transmitted to the
facial skull probably cause the face to bend and, to some extent, twist up against
its moorings” [Rosenberger, 1986, p. 791, and that this twisting is primarily resisted by bone in the interorbital region. According to Rosenberger, the primitive
primate skull exhibits a “cone-shaped” face, hafted onto the braincase a t its base
by a broad interorbital region medially, and the postorbital bars laterally. In
208 I Ross
contrast, the anthropoid skull is characterized by a short face with a highly reduced interorbital region. Reduction of the “interorbitum” reduces the skull’s ability to resist twisting of the face on the braincase during mastication and incision,
requiring the presence of a postorbital septum laterally to resist these stresses.
Rosenberger suggested that the trabeculated anterior accessory cavity of the anthropoid middle ear insulates the hearing apparatus from vibrations conducted by
the “heavily sutured and braced anthropoid skull.”
These hypotheses primarily address the most distinctive features of the anthropoid skull, the “forward-facing” bony orbits and the postorbital septum. The
functional and structural principles governing the evolution of the orbital region
have recently been elaborated [Cartmill, 1970, 1972; Kay & Cartmill, 1977; Ravosa, 1991; Ross & Ravosa, 1993; Ross, 1995a,bl and it is now possible to evaluate
and refine these hypotheses regarding the functions of these features in the anthropoid stem lineage. Some aspects of these models are confirmed, while others
are refuted. This paper presents a summary of these new data and a new explanation for the origin of Anthropoidea.
“he Structure of Adaptive Explanations
An adaptive explanation for anthropoid origins must explain why natural
selection would select for the defining features of anthropoids. Adaptations are
traits that have been fixed in a lineage by natural selection because they improved
the relative fitness of their possessors [Williams, 1966; Lewontin, 1978; Brandon,
1981, 1990; Gould & Vrba, 1982; Sober, 19841. Accordingly, an ideal “adaptation
explanation” [Brandon, 19901 should incorporate
“(1) Evidence . . . that some types are better adapted than others in the relevant selective environment (and that this has resulted in differential reproduction); (2) an ecological explanation of the fact that some types are better
adapted than others; (3) evidence that the traits in question are heritable; (4)
. . . information about patterns of gene flow and patterns of selective environments; and (5) phylogenetic information concerning what has evolved from
what . . .” [Brandon, 1990, p. 1651.
Because most evolutionary events, and certainly anthropoid origins, occurred
millions of years in the past, components (l),(3) and (4) of this “ideal” adaptation
explanation are usually not available. Explanations for the origins of specific features must utilize functionaVecologica1 analysis of trait function (component 121)
and phylogenetic information (component 151) to develop and test hypotheses.
Studies of trait function in extant animals serve to identify the functional principles governing how a feature functions and in what contexts. These functional
principles define the set of possible reasons for why the trait might have arisen.
Phylogenetic hypotheses can then be used to hypothesize as to the context in which
the trait actually arose, thereby defining the principles that were acting a t the
time [e.g., Kingsolver and Koehl, 19851.
According to this theoretical creed, our ignorance of anthropoid phylogenetic
relationships [see Fleagle and Kay, 19941 prevents us from determining the functions that these features served when they evolved. In this study, a new approach
to the explanation of anthropoid origins is attempted. Instead of using a phylogenetic hypothesis to define the context in which the distinctive anthropoid features
arose, and thereby determine which principles were acting at the time, the principles governing the functioning of the rare or unique features of anthropoids are
used to hypothesize the morphological and ecological contexts in which the features are most likely to have evolved. By focusing on their rare or unique features,
Strepsirhine
Anthropoid
Fig. 1. Diagrams illustrating differences in orbit orientation between strepsirrhines and anthropoids. Arrows
represent the orbital axes, although orbit orientation is measured using the orbital margin. Orbital convergence
is the degree to which the orbits face in the same direction (top figures). Strepsirrhines have less convergent
orbits than anthropoids. Frontation is the degree of verticality of the orbital margins. Strepsirrhines have less
frontated (vertical) orbital margins than anthropoids.
the rare or unique morphologicaVecologica1contexts characterizing the anthropoid
stem lineage can be reconstructed. These contexts can then be compared with those
predicted by competing hypotheses of anthropoid phylogenetic relationships.
FUNCTIONAL PRINCIPLES OF PRIMATE SKULL EVOLUTION
“Forward-Facing” Orbits
Anthropoids have long been observed to have more “forward-facing” orbits
than other primates [Clark, 19341. Orbit orientation can be defined in terms of
convergence, or the degree to which the orbits face in the same direction, and
frontation, or their degree of verticality (Fig. 1)[Cartmill, 19701. Measurements of
these variables in extant primates confirm that anthropoids have orbits that are
both more convergent and more frontated than those of prosimians [Ross, 1995al.
The reasons for this reside in the allometric and functional determinants of orbit
orientation.
Body size affects orbit orientation via its effects on relative orbit size. Orbit
210 I Ross
size scales with negative allometry against body size across all primates [Schultz,
1940; Kay and Cartmill, 1977; Martin, 19901,in part due to the negative allometry
of eyeball diameter across primates (indeed, across all vertebrates [Ritland, 19821).
Superimposed on the general negative allometry of orbit diameter are functional
factors relating to nocturnal versus diurnal activity patterns. Among small-bodied
visually oriented mammals, nocturnal animals have larger orbital apertures than
diurnal animals, but this is not true of animals above the size of Miopithecus
tulapoin,or Ototernur crussicaudutus (c. 1,300 g body weight and skulls length 75
mm) [Kay and Cartmill, 19771. One possible reason for this is that eye diameter
scales with negative allometry relative to orbit diameter [Schultz, 1940; Kay and
Cartmill, 19771, so that in larger animals the size of the orbital aperture is not
reflective of the size of the eye. Another possible reason is that larger animals have
eyes that are so large that they can contain both enough rods to allow nocturnal
activity and enough cones to facilitate diurnal activity. Whatever the reason,
small-bodied (<1,300 g) nocturnal mammals have relatively larger orbits than
small diurnal mammals, but relative orbit size is not influenced by activity pattern among larger animals.
Orbit size and orbit orientation. The negative allometry of relative orbit
diameter affects the two components of orbit orientation, convergence and frontation, differently. In animals with moderate degrees of orbital convergence, which
probably characterized the first primates, increases in relative orbit diameter are
predicted to result in decreases in orbital convergence [Cartmill, 19721. This is
corroborated by the comparative evidence: small-bodied primates have less convergent orbits than large-bodied animals [Ross, 1995al. Moreover, because smallbodied diurnal primates have relatively smaller orbits than small nocturnal primates they also have more convergent orbits (Fig. 2).
Once these allometric effects are taken into account, tarsiers, lorises and anthropoids are all revealed to have high degrees of orbital convergence [Cartmill,
1972; Ross, 1995al. In tarsiers and lorises this is attributable to nocturnal visual
predation [Cartmill, 1972; Allman, 1977; Pettigrew, 19781, but this explanation
cannot be applied to anthropoids. Although many anthropoids utilize visual predation to acquire food, the vast majority are not nocturnal visual predators: only
Aotus habitually forages for insects at night [Wright, 19893. Why then do anthropoids have more convergent orbits than prosimians at all body sizes?
The simplest explanation is one that invokes principles of allometry and utilizes the inferred primitive primate condition as a starting point. The earliest
primates were probably small-bodied nocturnal visual predators with moderate
degrees of orbital convergence [Cartmill, 19921. A shift to diurnality at small body
size in a descendent lineage would account for the high orbital convergence of
extant small-bodied anthropoids and the earliest anthropoids. Subsequent increases in body size in descendents of these small-bodied diurnal anthropoids
would have produced a further decrease in relative orbit diameter and a concomitant increase in convergence. This would account for the highly convergent orbits
of extant large-bodied anthropoids. The evolution of diurnality a t a body size above
1,300 g (and a skull length >75 mm) would not have been associated with a change
in relative orbit diameter and an increase in orbital convergence, and therefore
would not explain the full range of orbital convergence in anthropoids. This suggests that the stem lineage of extant anthropoids adopted diurnality at a skull
length of less than 75 mm and a body size of less than c.1,300 g [ROSS,1995al.
Allometric effects on frontation are more complex, but animals with relatively
large eyes and orbits tend to have intermediate degrees of frontation. This is
probably the only way they can fit large orbits in between the brain posterosupe-
0
0 0
0
0
0
0
Haplorhini
Strepsirhini
+
Rooneyia
Adapis
Leptadapis
0
i.
0
5
Microchoerus
Aegyptopithecus
10
15
20
25
30
Skull length (mm)
Fig. 2. Bivariate plot of orbital convergence and skull length in living and fossil primates. At small body sizes,
haplorhines (which are primarily diurnal) have more convergent orbits than strepsirrhines (predominantly
nocturnal).
riorly and the palate anteroinferiorly. However, allometry does not explain the
high degrees of orbital frontation in anthropoids [Cartmill, 1972; Ross, 1995aI:
there is no reason to believe that a simple reduction in relative orbit diameter
would produce an increase in orbital frontation, as suggested by Cartmill [19701.
Two alternate explanations for high frontation in anthropoids have been advanced [Ross,1994,1995al. The first suggests that increased basicranial flexion in
a lineage of animals with their orbits positioned close to each other (and to the
median sagittal plane) below the anterior portion of the basicranium would result
in increased orbital frontation. This hypothesis is supported by the observation
that animals with their orbits positioned close to the midline below the planum
sphenoideum display consistent covariation between the degree of frontation and
the degree of basicranial flexion, suggesting structural integration of the orbits
and anterior cranial base [Ravosa, 1991; Ross & Ravosa, 19931. The second hypothesis asserts that increases in frontal lobe dimensions alone would push the
superior orbital margin anteriorly, resulting in increased orbital frontation. This
hypothesis derives support from the observation that indriids, like anthropoids,
have both large frontal lobes [Radinsky, 19681 and very vertically oriented orbits
[Ross, 19931.
Both increased basicranial flexion and increased frontal lobe size may be related to a shift to diurnality. Across primates and haplorhines, increased flexion of
the basicranium is correlated with increases in both relative neurocranial volume
(a measure of brain size) and relative neocortical volume (the primary constituent
212 I Ross
of the frontal lobes) [Ross & Ravosa, 1993; Ross & Henneberg, 1995)’ Among
mammals, large relative brain size is correlated with diurnality [Jerison, 1973;
Eisenberg, 1975,19811; the only purely diurnal marsupial, Myrmecobius fusciutus,
has a relatively larger brain than other marsupials [Lee & Cockburn, 19851; the
diurnal tree shrews have relatively larger brains than insectivores, bats and most
nonsciurine rodents [Martin, 1990; Eisenberg, 19811, and the predominantly diurnal sciurines have relatively much larger brains than other rodents [Eisenberg,
19811. Relatively large brains have also been hypothesized to be advantageous to
frugivores, facilitating their monitoring of spatially and temporally disjunct fruit
resources, and to animals with large home ranges, accommodating the larger mental maps entailed by a living in a larger area [Clutton-Brock & Harvey, 1980;
Milton, 1988; Mace & Harvey, 19831. However, recent work suggests that when the
effects of group size are taken into account, frugivory and home range size are no
longer correlated with relative neocortex dimensions [Dunbar, 1992,1995; see also
Sawaguchi & Kudo, 19901. It would appear that group size is the most important
determinant of relative neocortex size.
Group living in primates is often argued to be an adaptation to obviate the
increased predation risks associated with diurnality [e.g., Van Schaik, 1983; Terborgh, 19831; certainly the diurnal strepsirrhines that live in groups (genus Eulemur, Propithecus and Zndri) have larger neocortex ratios than all other strepsirrhines except Loris and Nycticebus [Dunbar, 19921. Thus, it is reasonable to
suggest that the shift to diurnality a t small body size hypothesized for the anthropoid stem lineage would have been associated with a shift to group living, an
enlargement of the neocortex relative to the rest of the brain, and enlargement of
the brain overall. An increase in relative brain size would have resulted in increased basicranial flexion which, if occurring in a lineage of animals with their
orbits closely appressed to the midline below the olfactory tract, would have resulted in increased orbital frontation [Ross & Ravosa, 1993; Ross, 19931. Neocortex
is the primary constituent of the frontal lobes, so an increase in relative neocortex
size would have resulted in an increase in frontal lobe dimensions, in turn resulting in increased frontation of the orbital margins. Whether one or both of these
hypotheses is correct, adoption of a diurnal activity pattern in the stem anthropoids is expected to have been associated with increased orbital frontation.
Postorbital Septum
The postorbital septum of anthropoids, formed by the zygomatic, alisphenoid
and frontal bones, is otherwise found only in tarsiers. Some birds and some turtles
exhibit postorbital flanges behind their orbits, but they lack an alisphenoid bone,
so that only tarsiers and anthropoids among vertebrates have a zygomatic-alisphenoid contact behind the orbit. Various hypotheses have been advanced to explain
the origins of the postorbital septum. Cache1 [1979b] suggested that the septum
evolved to augment muscle attachment area for the anterior temporalis, and that
this additional anterior temporalis was utilized for incisal processing of large, tough
fruits. This hypothesis is difficult to accept in the light of data indicating that many
anthropoids do not have extensive areas of muscle attachment on the postorbital
septum, including those that engage in powerful incisor biting, such as Cebus and
‘There is no reason to believe that increased basicranial flexion is caused by enlarged eyes and orbits,
as suggested by Spatz [19681 and Cartmill [1970].This explanation for the “spatial-packing”problem
seen in tarsiers must be rejected.
the pitheciines [Ross, 1991,1995bl. Moreover, the anterior temporalis of humans,
macaques and owl monkeys is not recruited more than the masseter for powerful
incisor biting [Hylander & Johnson, 1985; Ross & Hylander unpublished data].
Rosenberger [19861 suggested that the postorbital septum functions to resist
tensile stresses acting on the skull during mastication or incision, but bone strain
recordings from the lateral orbital wall of Aotus suggest that during the power
stroke of incision and mastication the working-side postorbital septum is primarily
dorsoventrally compressed and “buckled,” a loading regime that would be better
resisted by a robust postorbital bar than a postorbital septum [Ross and Hylander,
19961. At present there is little reason to believe that the septum evolved to improve the structural integrity of the anthropoid face, as suggested by Rosenberger
[1986]. Greaves [1985, 19951 suggested that the postorbital septum evolved to
prevent twisting of the face on the braincase during mastication. However, once
again, the hypothesized loading regime does not obtain in extant anthropoids
[Hylander et al., 1991; Ross & Hylander, 19961, so the septum cannot be hypothesized to have performed that function.
Cartmill [19801 suggested that the postorbital septum evolved in the stem
lineage of tarsiers and anthropoids to insulate the eye, sensitized to nonconjugate
eye movements by the possession of a retinal fovea, from movements arising in
the temporal fossa during mastication. Most recently it has been suggested that
the postorbital septum evolved to protect the orbital contents from incursions
by the line of action of the anterior temporal muscles, muscles which curve around
the septum between origin and insertion [Ross, 1992, 1995131. This hypothesis
suggests that the orbital contour is in danger of being invaded by the anterior
temporal muscle fibers because of increased orbital frontation and convergence in
early anthropoids. Because the anterior temporal muscles take origin from the
uppermost portion of the septum (on the frontal bone) and the adjacent temporalis
fascia, muscle position relative to the orbital contents is affected by changes in
orbit orientation. When marked orbital convergence and frontation are combined,
the temporal musculature is in danger of invading the orbit from behind, necessitating the presence of a postorbital septum.
Either of these hypotheses is compromised by the existence of other ways of
protecting the orbital contents [Ross, 1995bl. One way is to decrease the size of the
anterior temporal musculature, thereby creating more space between the periorbita and the temporal muscles. However, this would reduce the mass of a catholically recruited jaw adductor [Ross and Hylander, unpublished data] with the
longest lever arm and most vertical orientation of any of the masticatory muscles.
Another option is to decrease relative eye size, thereby creating more room in the
orbit and enabling the eye and its adnexa to be separated from the temporal fossa
by intraorbital fat and connective tissue septa [Koorneef, 19921. However, reduction in the size of the eye relative to the orbit is unlikely to be an option at small
body sizes (below c. 1,300 g) when eye size is at a premium. This is particularly the
case for small diurnal animals that need to maintain eyes with a relatively long
focal length and a relatively large retina lying close to the temporal fossa. These
considerations suggest that if the septum evolved to insulate the orbital contents
from temporal muscles rostrally positioned by high orbital convergence and frontation, this is most likely to have occurred in small-bodied animals that needed to
maintain bite force magnitudes andlor visual acuity.
Retinal fovea
Retinal foveae occur in many vertebrates, but the only mammals with a fovea
are tarsiers and anthropoids. In all vertebrates the fovea consists of a pit in the
214
I Ross
inner' layers of the retina vovea is Latin for pit), a relatively higher density of
photoreceptors than in other parts of the retina, and a relatively lower ratio of
photoreceptors to ganglion cells. In tarsiers and anthropoids the blood vessels are
also deflected away from the fovea [Walls, 1942; see Martin, 1985 for birds]. A
range of fovea shapes has been identified, from steep-sided (convexiclivate)foveae,
to shallow-sided (concaviclivate) foveae. Most haplorhines have concaviclivate
foveae, only Callithrix jacchus displaying a fovea that even approaches the convexiclivate condition of birds of prey [Rohen & Castenholtz, 19671. The likely
function of the fovea in ancestral tarsiers and anthropoids can be inferred from
data on the dioptrics of the eye and the distribution of different fovea types among
other vertebrates.
Dioptrics. The high density of photoreceptors and the low photorecept0r:ganglion cell ratio yield high visual acuity by increasing the resolution of the image
received by the retina and transmitted to the brain. The deflection of the retinal
blood vessels away from the fovea in haplorhines also increases visual acuity by
removing potentially refractive tissues from the path of the incoming light rays
[Ohm et al., 19721. This function is particularly necessary in the area centralis, in
which the fovea is situated, because the low receptor:ganglion cell ratio in the area
results in a great thickening of the retinal tissues lying inside the photoreceptor
layer [Hughes, 19771. This thickening of the retina in the area has the deleterious
effect of making the retinal surface convex, focusing the incoming light rays on a
smaller area of photoreceptors and reducing image size. Walls 119421 suggested
that the fovea functions to counter this effect of retinal convexity by refracting
incoming light rays away from the perpendicular to the surfaces of the fovea,
enlarging the image that falls on the photoreceptors and thereby increasing visual
acuity [Walls, 1937, 19421.
Walls 119421 considered concaviclivate foveae to be degenerate forms "descended" from the convexiclivate foveae of their respective ancestors. Because
Walls associated the convexiclivate foveae with diurnality, his theory explained
the concaviclivate foveae of nocturnal animals (owls and Sphenodon) as primitive
and degenerate retentions from diurnal ancestors. Walls might similarly have
explained the concaviclivate fovea of Tarsius in an all-rod retina as a degeneration
of that of a diurnal ancestor, as is implicit in recent treatments [Cartmill, 1980;
Ross, 19931. However, Walls's explanation does not explain the presence of concaviclivate foveae in diurnal animals such as anthropoids, and more recent work
suggests that convexiclivate foveae provide enhanced sensitivity to movement a t
the cost of decreased visual acuity [Pumphrey, 19481. This suggests that concaviclivate foveae provided increased acuity where great sensitivity to movement is
not required, perhaps for the detection of cryptic prey as suggested by Cartmill
119801.
Distribution of vertebrate foveae. Most nonanthropoid foveate vertebrates,
whether possessed of concaviclivate or convexiclivate foveae, whether nocturnal or
diurnal, are visual predators (Table I). The most obvious examples are the predatory birds, both nocturnal and diurnal, the deep sea fish Bathylagus and Bathytrocytes [Vilter, 1954; in Lockett, 19773, Sphenodon, the diurnal bird-eating tree
snakes (Dryophis),chameleons, and Tarsius. However, lizards, the littoral teleosts
and water birds are also visual predators, and most adult birds at least catch prey
for their offspring, if not for themselves. Certainly most of the passerines are
'When talking about the eye, inner means towards the center of the eye.
TABLE.I. Distribution of Foveae Among Vertebrates
Taxon
Teleosts
Some deep water teleosts (searsides,
alepocephalids and scopelosaurids)
[Lockett, 19771
Some littoral teleosts [Walls, 19421
Reptiles
Sphenodon [Walls, 19421
One Chelonian, Amy& [Walls, 19421
Most diurnal lizards
Three genera of diurnal snakes
Dryophis, Dryophiops, Thelotornis
[Walls, 19421
Birds [Walls, 19421
Most birds
Some ground-feeders, many
swimmers, divers and waders
Hawks, eagles, swallows, terns,
kingfishers, bitterns, humming birds,
some wing-feeding passerines
Some gulls, shearwaters, flamingo
Owls, Apus apus, Strigops
ha broptilus
Mammals
Tarsius
Anthropoidea (except Aotus)
Nocturnal/
diurnal
Type of fovea (steepness)
Various
concaviclivate (Bathytrocytes,
Bathylagus) convexiclivate
(pure rod)
concaviclivate to convexiclivate
Nocturnal
Diurnal
Diurnal
Diurnal
medium (pure rod)
concaviclivate
concaviclivate to convexiclivate
medium
Diurnal
medium
Diurnal
Diurnal
Diurnal
Nocturnal
concaviclivate
two foveae: central one
convexiclivate, temporal one
concaviclivate
linear fovea
concaviclivate, sometimes none
Nocturnal
Diurnal
concaviclivate (pure rod)
concaviclivate
“Nocturnal”
insectivorous to some degree. These comparative data suggest that the concaviclivate fovea seen in most haplorhines can be hypothesized to have evolved in response to selection for high visual acuity used for visual predation.
The function of the fovea in extant anthropoids and tarsiers. Visual
predation of insects is not usually thought of as a characteristic of Anthropoidea,
the majority of which include large proportions of fruit in their diets. However,
small-bodied anthropoids spend significant amounts of time searching for insects
and other small invertebrates (Table 11). Even many larger-bodied anthropoids
utilize insects as an important source of protein (Table TI) [Garber, 1992;Janson &
Boinski, 1992; Terborgh, 1983; Robinson & Janson, 1987; Struhsaker, 19781, although body size-related constraints mean that generally only small-bodied mammals (5350g) can survive solely on insects. This is because increases in body size
are associated with significant increases in the amount of insect material required,
but without appreciable increases in the size of insect prey. Thus, body sizes above
c. 350 g are associated with unrealistically high numbers of successful insect captures necessary per hour [Kay & Covert, 19841. Saimiri is the largest anthropoid
[c. 1,000 g, Ford & Davis, 19921 that gleans the majority of its prey from exposed
surfaces, spending most of its time foraging for insects as it migrates between fruit
trees. Saimiri may therefore delineate the uppermost body size a t which the haplorhine fovea is likely to have evolved as an adaptation for visual predation of
exposed insects. Larger anthropoids do spend significant amounts of time foraging
for insects, e.g., Cebus apella and C . albifrons, but they are not visual predators,
216 I Ross
obtaining the majority of their prey via destructive foraging for hidden prey [Terborgh, 1983; Robinson & Janson, 19871.
In sum, most vertebrates with retinal foveae are diurnal visual predators,
suggesting that the portion of the anthropoid stem lineage in which the fovea
evolved consisted of diurnal visual predators. The importance of visual predation
on insects in the foraging repertoire of extant small anthropoids and the utilization
of insects by many larger anthropoids, corroborate this hypothesis. The relationship between prey capture rates and body size, in the context of the data on
Saimiri, suggests that the evolution of the fovea for diurnal visual predation is
most likely to have occurred in animals weighing less than 1,000 g. The concaviclivate shape of the haplorhine foveae suggests that movement detection was not
its original function.
THE CONTEXT OF ANTHROPOID ORIGINS
The functional and structural principles governing the evolution of the anthropoid postorbital septum, orbital convergence and retinal fovea suggest specific
ecological and morphological contexts in which these features are most likely to
have evolved. These contexts are summarized in Figure 3. It is hypothesized here
that the postorbital septum of anthropoids evolved as an adaptation to protect the
orbital contents from encroaching fibers of anterior temporalis and that this encroachment was due to the combination of high orbital convergence and frontation
in a lineage of small-bodied animals with relatively large eyes. Increasing orbital
convergence is hypothesized to have been due to a reduction in relative orbit
diameter associated with a shift to diurnality at a body size below about 1,300 g or
a skull length below c. 75 mm. Increased orbital frontation is hypothesized to have
been due to increases in the size of the brian, particularly the neocortex, resulting
in rostra1 displacement of the superior orbital margin andlor increasing basicranial flexion in a lineage of animals with orbits closely appressed to the midline
below the basicranium. The retinal fovea is hypothesized to have evolved in a
lineage of small-bodied animals as an adaptation to diurnal, visually directed
insect predation. All these features are hypothesized to have evolved in association
with a shift from nocturnal to diurnal visual predation of insects a t small body size
and this adaptive shift is argued to be the defining feature of the anthropoid
suborder.
Some of these events are causally interrelated and are therefore predicted to
have occurred simultaneously, while others may have happened earlier or later.
The postorbital septum is hypothesized to have evolved at the same time that the
orbits became both highly convergent and highly frontated3. Increased orbital
convergence almost certainly evolved a t the same time as the shift to diurnality
because all small diurnal primates have relatively smaller and more convergent
orbits than similarly sized nocturnal primates. Increased frontation, due to increasing neocortex, and brain size associated with selection for group-living, is also
hypothesized to have occurred at the same time as the shift to diurnality. Consequently, increased orbital convergence, increased orbital frontation and the postorbital septum are all hypothesized to have evolved simultaneously as the ancestral anthropoids adopted diurnal habits.
3The septum is not predicted in the context of only one of these features;highly frontated orbits that face
sideways do not necessitate a septum [e.g., tree shrews], nor do highly convergent orbits that face
upwards [e.g., Lorisl.
TABLE 11. Time Spent Foraging for Insects by Anthropoids
SDecies
Callithrix flaviceps and C .
jacchus
Saguinus spp.
Saguinus fuscicollis
Saimiri sciureus (Surinam)
Saimiri sciureus (Peru)
Cebus olivaceus (Venezuela)
SdY
weight (e)"
Estimate of 8
insects in diet
%
Methodsb
Reference'
310
24-30
Time
Rylands & de Faria [19931
400-740
462
960
30-77
16
72
82
55.4
35.1
37
33.3
30-51
20
47.3
75.4
63.6
20
15
11
1
12-17
14
10
3
25
21.8
Time
Time
TF
TF
TF
Time
Time
Garber [19931
Terborgh [1983]
Robinson and Janson [19871
Robinson and Janson 119871
Robinson et al. [1987]
Robinson et al. [19871
Robinson et al. [19871
Robinson et al. I19871
Robinson et al. [1987]
Waser [19771
Aldrich-Blake [19801
Cords [19871
Cords [19871
28.6
Time
Cords [19871
12.6
24.5
16.8
19.8-37.7
13
4.9
9.6
16.1
some
some
1
25
13
2
1
1-15
(stomach)
Time
Time
Time
Time
(stomach)
(stomach)
(stomach)
3,500
Cebus olivaceus (Surinam)
Cebus capucinus (Costa Rica)
Cebus capucinus (Panama)
Cebus apella (Surinam)
Cebus apella (Peru)
Cebus albifrons (Peru)
Cebus albifrons (Colombia)
Aotus trivirgatus (Peru)
Aotus tivirgatus (Paraguay)
Callicebus moloch (Peru)
3,500
3,700
Callicebus torqmtus (Peru)
Cercocebus albigenn (?)
Long-tailed macaque (Malaysia)
Cercopithecus ascanius (Kenya)
Cercopithecus ascanius
(Uganda)
Cercopithecus ascanius
(Uganda)
Cercopithecus cephus (Gabon)
Cercopithecus diann (Ghana)
Cercopithecus mitis (Kenya)
Cercopithecus mitis (Uganda)
Cercopithecus mitis (Zaire)
Cercopithecus neglectus (Gabon)
Cercopithecus nictitans (Gabon)
Cercopithecus pogonias (Gabon)
Cercopithecus l'hoesti (Uganda)
Erythrocebus patus (Uganda)
Hylobates agilis (Malaysia)
Hylobates klossi (Indonesia)
Hylobates Iur (Malaysia)
Hylobates muelleri (Malaysia)
Hylobates pikatus (Thailand)
Hylobates syndoctylus
(Malaysia)
Hylobates syndoctylus
(Indonesia)
Pongo p y g m u s
Gorilla gorilla
1,490
8,980
3,300
3,260
1,220
1,070
4,170
4,000
6,320
6,500
4,500
11,100
5,830
5,670
5,700
5,760
10,900
13
F
IT
TF
TF
II
TF
TF
TF
Tr
TF
TF
Tr
TF
Tr
Time
Time
Time
Time
Time
Time
Cords [19871
Cords 119871
Cords [19871
Cords [19871
Cords [19871
Cords [19871
Cords [19871
Cords [19871
Cords [19871
Cords 119871
Leighton [1987]
Leighton 119871
Leighton El9871
Leighton [19871
Leighton 119871
Leighton [1987]
Time
Leighton [1987]
Q
Q
81,000
169,500
some
seldom
Q
Q
Pan troglodytes
60,000
Time
Pan paniscus
45,000
4-23 (vert. and
invert.prey)
some vert.
and invert.prey
Q
Rodman and Mitani [19871
Stewart and Harcourt
[19871
Nishida and
Hiraiwa-Hasegawa [19871
Nishida and
Hiraiwa-Hasegawa [19871
"From Fleagle [19881.
bNote that proportions were estimated by various researchers using various methods of data collection so
percentages cannot be used for interspecific comparisons. They are merely intended to demonstrate that insects
constitute a significant proportion of the diets of many anthropoids. IT,time-taking method: records the proportion of time spent feeding on insects; TF, time-foraging method: records the time spent foraging for and
feeding on insects; 11, items ingested: records estimated weights of different prey items ingested, F, frequency:
frequency with which different items were taken; Time, proportion of daily time budget allocated to insect
foraging; Q, qualitative estimate.
cNames given are principally references for reviews of the literature, not for authors of the original work.
218 I Ross
Ancestral
High
High
anthropoid
orbital
orbital
condition
convergence frontation
Postorbital
septum
Fovea
Context
Ancestral
condition
Fig. 3. Diagram illustrating the contexts in which the distinctive anthropoid features (top) would arise in
descent from the ancestral primate condition. The dark box indicates a nocturnal activity pattern for the
ancestral form; the white areas indicate diurnality for early anthropoids. See text for details.
These changes are hypothesized to have occurred after the evolution of highly
approximated orbits. Cartmill [19701 also posited that the group of prosimians
which gave rise to anthropoids displayed “an apical interorbital septum” because
he envisaged subsequent reduction in relative orbital diameter associated with a
shift to diurnality to have resulted in a n expansion of the brain out over the nasal
fossa. However, Cartmill failed to specify how the orbits came to be closely approximated in the first place, why a reduction in relative orbit diameter would be
associated with a n increase rather than a decrease in orbital frontation, and why
the brain would have expanded out over the orbits just because the orbits became
more frontated.
The most common cause of orbital approximation among primates is orbital
enlargement resulting allometrically in intermediate degrees of orbital frontation.
Such a condition is seen in Galago moholi senegalensis, which has large, moderately frontated and convergent orbits [Ross, 1995al and a small area where the
medial orbital walls are in contact [Simons & Rasmussen, 19891. More extensive
contact of the medial orbital walls below the olfactory tract combines with moderate frontation in Tarsius. If the anthropoid stem lineage had their orbits closely
approximated below the olfactory tract, not only would increasing neocortical volume have been accommodated by expansion of the brain out over the orbits, but
increases in basicranial flexion in their descendants would have been associated
with increases in orbital frontation. For these reasons, a combination of enlarged
orbits, moderate orbital frontation and convergence and orbital approximation
below the olfactory tract is argued to have preceded the shift to diurnality and the
evolution of pronounced orbital convergence in the anthropoid stem lineage. Pronounced orbital frontation in that stem lineage is argued to have been due to
Anthropoid Origins / 219
increasing relative neocortex volume concurrent with the shift to diurnality and
not due merely to decreasing orbital diameter as suggested by Cartmill [19701.
Cartmill [19801 suggested that the postorbital septum and retinal fovea
evolved as a single adaptation, implying that they evolved simultaneously. He
argues that the retinal fovea evolved as an adaptation for diurnal visual predation
on cryptic insects and the septum evolved to allow stem haplorhines to chew one
insect while foraging for the next. Although possession of a fovea would have made
the eyes of stem anthropoids more sensitive to nonconjugate eye movements,
thereby enhancing the probability of evolving a postorbital septum, it could also be
argued that possession of a postorbital septum enhances the probability of the
evolution of a fovea because it increases the stability of the eyes. The model advanced here provides a mechanism whereby the retinal fovea could have evolved
independently of the postorbital septum. Because the postorbital septum is argued
to have evolved simultaneously with a shift from nocturnality to diurnality and
the retinal fovea is unlikely to have evolved in a nocturnal environment, the fovea
either evolved simultaneously with, or subsequent to the shift to diurnality.
Anthropoid Evolution and Relationships
How does the hypothesis that the defining features of anthropoids evolved in
association with a shift from nocturnal to diurnal visual predation of insects at
small body size fit in with the fossil record of early anthropoid evolution? The
oldest well-known undisputed fossil anthropoids are the parapithecoids and oligopithecines from the Late Eocene of North Africa. These animals were small (Qatrania wingi, 300 g; Apidium moustafai, 600 g; Oligopithecus savagei, 700 to 1,000
g; 0. rogeri, 1,300 g; Catopithecus browni, 600 to 900 g), diurnal, insectivore/
frugivores with a postorbital septum [Kay & Simons, 1980; Simons & Kay, 1983;
Simons, 1990; Rasmussen & Simons, 1988,1992; Simons & Rasmussen, 19941. The
preserved contours of the orbital rims in DPC 8772 and 42222 indicate that Catopithecus’s orbits were convergent, at least moderately frontated and most closely
approximated below the olfactory tract, although how closely is impossible to say
for sure. Catopithecus’s molar morphology and that of the other oligopithecines
suggests that they “were considerably less committed to frugivory than the parapithecids and propliopithecines were” [Rasmussen & Simons, 1992, p. 15; see also
Gheerbrant et al., 19951.
Unfortunately, the fossil evidence does not allow us to determine whether
early anthropoids had increased orbital frontation because of increased brain size
relative to basicranial length, resulting in increased basicranial flexion, or because of enlarged frontal lobes. Although the earliest small-bodied anthropoids for
which estimates are available appear to have had relative brain sizes below those
of extant forms [Catopithecus and Apidium phiomense: Fleagle & Rosenberger,
1983; Radinsky, 1977; Rasmussen & Simons, 1992; Simons, 1993; Simons & Rasmussen, 1994; Simons, 19951, it is brain size relative to basicranial length that is
the important determinant of the degree of basicranial flexion [Ross & Ravosa,
19931. These variables are unknown for these early anthropoids. Until basicranial
length, basicranial flexion or frontal lobe sizelshape are known for early anthropoids, the question of why their orbits were moderately frontated will remain
unanswered.
A newly discovered family of primates from China, the Eosimiidae, has been
claimed to be the earliest anthropoids [Beard et al., 1994, 1996; Dagosto et al.,
1996; Gebo et al., 19961, although they may also be stem haplorhines, or the sister
taxon of a tarsier-anthropoid clade (Kay et al, submitted). To date, no cranial
remains have been recovered that would enable the activity patterns of these
220 I Ross
putative stem anthropoids to be estimated. However, it is clear that Eosimias
centennicus had small, vertically implanted lower incisors associated with a vertically oriented but unfused mandibular symphysis [Beard et al., 19961. The extensive cresting on the molars and the small size of Eosimius (90-180 g for E .
centennicus) suggest that these animals had a diet consisting of extensive amounts
of insect prey. If eosimiids are indeed early anthropoids or stem haplorhines, their
morphology corroborates the hypothesis advanced here: that early anthropoids
were small-bodied insectivorous animals.
If the animals that gave rise to anthropoids were small (<1,000 g) nocturnal
visual predators with orbits that were relatively large, moderately frontated and
convergent, and closely approximated below the olfactory tract, this has several
implications for hypotheses regarding anthropoid relationships. First, the ancestors of anthropoids as reconstructed in this study bear close morphological resemblance to many omomyids but to few known adapids [Ross, 19941. Most omomyids
are small, nocturnal, visual predators with moderately convergent and frontated
bony orbits that are pressed close to the midline below the anterior cranial fossa.
The only adapids presently known to have been small, nocturnal, and probably
visual predators are the cercamoniines Pronycticebus gaudryi [Simons, 19721 and
Caenopithecus neglectus [Franzen, 19941. The orbits of Pronycticebus gaudryi are
moderately convergent and frontated, but they are separated by a significant distance [Szalay & Delson, 19791, suggesting that increased basicranial flexion or
frontal lobe size in such an animal would be unlikely to result in increased orbital
frontation. Although the teeth of cercamoniines resemble those of early anthropoids in some respects [Rasmussen, 1994; Simons, 19951 the most extensive analysis of dental evidence for anthropoid origins found a cercamoniine-anthropoid
clade highly unparsimonious [Kay & Williams, 19941. Attempts to derive anthropoids from adapids therefore not only face the difficulty of explaining away numerous similarities shared by anthropoids, omomyids and tarsiers [Ross, 1994;
Kay & Williams, 19941 (see below), but they also lack an adapid with the skull
morphology appropriate for an anthropoid ancestor. Second, the omomyid cranial
features suggested here to have been critical antecedent conditions for the evolution of the anthropoid skull (large, moderately convergent and frontated orbits
closely approximated below the olfactory tract) are widely distributed among omomyids. This suggests that these features were present in the last common omomyid
ancestor, providing little reason to prefer omomyids over basal primates as anthropoid ancestors. Thus, the morphotype suggested in this study to have given
rise to anthropoids closely resembles the earliest primates reconstructed by Cartmill [1992] and Sussman [19911. Indeed, if basal primates exhibited not only moderate degrees of orbital convergence and nocturnal habits, but also moderately
frontated orbits that were pressed close to the midline below the anterior basicranium, they could easily have given rise to the anthropoid stem species simply by
adopting a diurnal activity pattern.
Finally, there is much debate over the relationships of tarsiers to other primates. Much of this debate centers around the question of the homology of two of
the features discussed here: the postorbital septum and the retinal fovea. Tarsiers
and anthropoids are the only mammals that possess these features. Moreover, they
are also the sole possessors of some unusual features of the ear region. Consequently, tarsiers and anthropoids have been argued to be more closely related to
each other than to any other primates, living or fossil [Cartmill & Kay, 1978;
MacPhee & Cartmill, 1986;Ross, 19941. If anthropoids and tarsiers inherited their
postorbital septa from a common ancestor and this ancestor evolved the postorbital
septum in the context outlined above, then tarsiers must have a small, diurnal,
Anthropoid Origins / 221
visual predator stage in their ancestry. This has the advantage of explaining why
tarsiers possess a retinal fovea and lack a tapetum [Cartmill, 19801. Loss of the
tapetum in turn explains why tarsiers evolved their characteristically enormous
eyes with reinvasion of the nocturnal niche. Finally, the anterior temporal muscles
of tarsiers curve around the postorbital septum, suggesting that only because they
have a postorbital septum can tarsiers have such enormous, moderately convergent and frontated orbits [Ross, 1995bl. Only the postorbital septum prevents their
eyes from bouncing around when tarsiers chew.
The claim that Tursius is more closely related to Anthropoidea than any other
primates, living or fossil, is difficult to reconcile with the claim by some workers
that the omomyid, Shoshonius cooperi, is the sister taxon of Tursius [Beard et al.,
1991;Beard & MacPhee, 19941. However, a Shoshoniw-Tursius clade is supported
by only one feature that is not also found in other omomyids: extreme enlargement
of the orbits [Ross, 19941. All of the other features argued to be tarsier-Shoshonius
synapomorphies are also found in other omomyids, when preserved [Ross, 19941.
The following scenario seems more likely (Fig. 4). Primates arose as a lineage
of small, nocturnal, visual predators eating a combination of insects and fruits in
the shrub layer of tropical rainforests [Cartmill, 1992; Sussman, 19911. These
animals had relatively enlarged, moderately convergent orbits, a tapetum lucidum
and a retina dominated by rods. A small number of cones inherited from their
primitive mammalian ancestors [Jacobs, 1994153 served to regulate activity patterns [Martin, 19901. Although possessing slightly larger brains than other mammals at the time, these early primates had relatively smaller brains than extant
primates. They avoided predation by moving stealthily and solitarily through the
shrub layer. Omomyids closely resemble the putative primitive primates in morphology and inferred ecology.
Some time after the origins of primates, a lineage of small-bodied (<1,000 g)
descendents with their orbits pressed close together below the olfactory tract
adopted a diurnal activity pattern while continuing to be visual predators and
frugivores. These were the ancestors of haplorhines, i.e., tarsiers and anthropoids.
This shift to diurnality was accompanied by a number of behavioral and morphological changes. These stem haplorhines began living in family groups to reduce
the increased predation risks attendant upon diurnality. Group living was associated with increases in brain size, particularly of the neocortex, which resulted in
an increase in orbital frontation. Simultaneously, the shift to diurnality resulted
in a decrease in relative orbit diameter and an increase in orbital convergence. As
orbital convergence and frontation increased, the anteriormost fibers of anterior
temporalis were dragged rostrally towards the eye and a postorbital septum developed from the frontal, zygomatic and alisphenoid bones in order to protect the
orbital contents from movements in the anterior temporal fossa. Such protection
would have enabled these early haplorhines to forage for one insect while chewing
the last [Cartmill, 19801, to monitor the actions of other group members, or to
monitor their environment for predators while chewing. The shift to diurnality
also necessitated the loss of the tapetum lucidum, an increase in the number of
cones, and the evolution of a retinal fovea in order to improve visual acuity needed
for detection of cryptic insects.
These stem haplorhines faced significant competition from diurnal birds (see
below). One lineage of haplorhines, unable to compete successfully, reverted to
nocturnality and became tarsiers. Lacking a tapetum lucidum to enhance visual
sensitivity in low light levels, these ancestral tarsiers evolved relatively enormous
eyes and an all rod retina to enable them to be effective nocturnal visual predators.
These enormous eyes crowded back into the temporal fossa, restricting the area of
222 I Ross
Fig. 4. Evolutionary tree illustrating primate phylogeny and evolutionary scenario hypothesized here. See text
for details.
origin for the medial pterygoid muscle, forcing one head of the muscle to take
origin from the medial wall of the orbit. A thick, tense fascia evolved to prevent
this muscle from bulging against the orbital contents during mastication [Ross,
1995bl. Inherited from a diurnal ancestor, the postorbital septum protected the
orbital contents from the anterior temporalis muscle, enabling these early tarsiers
to have orbits that bulged back into the temporal fossa while remaining highly
convergent for their size. High orbital convergence provided the improved image
quality at low levels necessary to nocturnal visual predators [Allman, 1977; Pettigrew, 19781.
The other lineage of haplorhines, the Anthropoidea, remained diurnal. Managing to compete successfully with birds, they radiated and filled the small, diurnal, arboreal, tropical mammal niche. Insectivory remained important in many
lineages (e.g., oligopithecines) while frugivory was adopted by others (e.g., parapithecoids, propliopithecids, Algeripithecus). Subsequent increases in body size saw
further increases in orbital convergence and the spread of anthropoids to niches
outside the tropical rainforest and to places outside the place of origin. Anthropoids
were soon present in Africa, South America and Asia where sympatric prosimians,
if present, were confined to nocturnal ecological niches. Only on the island of
Madagascar, where strepsirrhine prosimians were isolated from anthropoids, did
prosimians evolve diurnal activity patterns. Generally, because diurnality among
strepsirrhines evolved at large body size, they did not evolve the extreme orbital
convergence seen in large-bodied anthropoids, nor the relatively large brains associated with group living4.
How to be a Small, Insectivorous, Diurnal, Arboreal, Tropical Mammal
Diurnal, small-bodied, arboreal mammals are rare in tropical ecosystems
[Charles-Dominique, 19751. Indeed, the only small (<1,000 g), diurnal, predominantly arboreal mammals are anthropoid primates, some tree squirrels and tree
shrews [Nowak, 19911. Charles-Dominique [19751 attributed this to competition
with tropical rainforest birds, most of which are diurnal. He suggested that mammals only managed to be both diurnal and arboreal in competition with birds by
adopting large body size, continuously growing incisors, claws, and intelligence
[Charles-Dominique, 19751.
Certainly the large body size ofdlouatta,Ateles and Lagothrix enables them to
eat significant proportions of leaves, exploiting a niche not utilized by birds. However, anthropoids and birds also appear to compete for many of the same resources,
displaying remarkable morphological convergence as a result. At Cocha Cashu, 25
species of bark-foraging insectivorous birds, primarily woodcreepers (Dendrocolaptidae), forage for insects on large vertical supports, possibly in competition with
Saguinus fuscicollis [Terborgh, 19851. Like callitrichids, woodcreepers and woodpeckers use climbing adaptations, strong tails, large sharp claws and reduced
halluces, to climb on trunks and large branches where they rip bark and tap wood
in search of insects [Storer, 19711. Marmosets and tamarins compete with 94 species of understory or shrub layer avian insectivores a t Cocha Cashu that obtain
their prey from foliage surfaces [Robinson and Terborgh, 19901. Like almost all
diurnal birds, these avian insectivores possess a retinal fovea, used for visual
predation of exposed insects [Walls, 1942; Martin, 19851. Large “folivorous” anthropoids compete with 88 species of frugivorous or omnivorous canopy-dwelling
birds for the large quantities of fruit pulp they both eat each day [Robinson and
Terborgh, 19901. Many birds also possess flanges of bone extending laterally from
the braincase behind the orbits which appear to deflect the M. adductor mandibulae externus rostralis temporalis around the eye, much as the postorbital septum
deflects the anterior temporal muscles in anthropoids.
Extant anthropoids may also exist side-by-sidewith birds by utilizing different
classes of tropical fruits. Janson [19831 observed that in a Peruvian tropical forest,
anthropoids eat primarily large orange, yellow, brown or green fruits with a husk,
whereas birds eat small, red, black, white, blue, purple or mixed-color fruits without a husk. Janson associated these dietary differences with differences in size,
visual ability and morphology of the masticatory apparatus. Janson noted that
most of the frugivorous birds in Peru weigh less than 200 g and have a high
sensitivity to a wide range of colors whereas anthropoids range from 400 to 8,000
g and can see green, yellow and orange but cannot discriminate or identify reds.
Finally, birds “have little ability to manipulate fruits with precision” [Janson,
1983, p. 1891, whereas anthropoids have powerful jaws, “complex teeth and manipulative tongues.” Primates also possess powerful manipulative hands.
The fossil record of early anthropoids suggests that Janson’s hypothesis might
explain how oligopithecines, parapithecoids and propliopithecids competed with
sympatric birds. These anthropoids were small, with rooted spatulate upper inci-
4The ring-tailedlemur, Lemur cum, is the smallest diurnal strepsirrhine,weighing in at c. 2,600 g. This
is twice the largest size at which the anthropoid stem lineage is hypothesized to have adopted diurnality.
224 I Ross
sors, unspecialized lower incisors, small brains [Simons & Rasmussen, 1994;Simons, 19951 and with no indications of specialized postcranial adaptations such as
claws that might have assisted them in competing with birds [Gebo et al., 19941.
However, oligopithecines (600-1,300g) parapithecoids (300-3,000g) and propliopithecids (4,000-6,700g) resembled extant platyrrhines in being generally larger
than frugivorous birds and in having powerful jaws and teeth adapted, a t least in
part, for frugivory [Fleagle, 19881.Like all recent anthropoids, parapithecoids and
propliopithecids also possessed fused mandibular symphyses5, enabling greater
amounts of balancing-side muscle force to be transferred to any bite point, facilitating more powerful mastication and incision [Ravosa and Hylander, 19941.In
combination with robust incisors, symphyseal fusion would have enabled these
early anthropoids to exert powerful bites on hard, husked fruits. Thus, these late
Eocene-early Oligocene anthropoids may have avoided competition with birds by
exploiting hard, husked fruits requiring powerful incisal, and possibly manual,
preparation.
However, these arguments are difficult to extrapolate back to the earliest
haplorhines that first made the transition from nocturnal to diurnal visual predation. Predation of large hard fruits rather than small soft ones is an implausible
explanation for the presence of a retinal fovea. Moreover, studies of the evolution
of primate color vision suggest that primate trichromacy only became fixed in the
catarrhine lineage after their divergence from platyrrhines: early haplorhines
were more than likely dichromatic, or polymorphic at best [Jacobs, 199461.Moreover, if eosimiids are either stem haplorhines or early anthropoids, they lack the
molar morphology usually indicative of frugivory among primates. Rather, like the
stem haplorhines hypothesized here they instead appear to have been insectivorous. It remains to be determined how the first small diurnal insectivorous haplorhine visual predators might have competed with sympatric insectivorous birds.
Studies of sympatric communities of extant anthropoids and birds would be useful
in this regard.
CONCLUSIONS
The precise time and place of haplorhine origins remain unknown but evidence
from comparative anatomy and data from the fossil record can be used to reconstruct the context in which the distinctive anthropoid features arose, a shift to
diurnal visual predation of cryptic insects at small body size. This hypothesis
explains the origins of the retinal fovea, extreme orbital convergence and frontation, increased neocortical volume, and, indirectly, the origin of the postorbital
septum. The animals that gave rise to haplorhines resembled primitive primates
in being small-bodied nocturnal visual predators with a moderate degree of orbital
convergence. Later anthropoids probably managed to compete with birds by utilizing hard, husked fruits opened with robust incisors and manipulative hands.
How early insectivorous haplorhines competed with diurnal insectivorous birds
remains to be shown.
If tarsiers and anthropoids are both descended from the same small-bodied,
diurnal visual predator, this would explain why tarsiers are nocturnal yet possess
a retinal fovea and lack a tapetum lucidum. It is likely that such an animal could
only reinvade the “nocturnal visual predator” niche by evolving enormous eyes to
capture as much incoming light as possible [Cartmill, 19801. This in turn was
51t is not clear whether or not Catopithecus had a fused mandibular symphysis. [Simons, 19951.
probably only possible in the presence of a postorbital septum, making this septum
a true evolutionary innovation. There is ample evidence from the dentition and
skull of tarsiers and anthropoids to suggest that the two are sister taxa [Ross, 1994;
Kay & Williams, 19941 and the present study strengthens this hypothesis by demonstrating that many of the features shared by tarsiers and anthropoids were most
likely evolved in a small-bodied diurnal visual predator. It is unparsimonious to
assume that tarsiers and anthropoids each passed through such a stage independently, suggesting that the shift to such an adaptive zone explains the origins of a
tarsier-anthropoid clade, Haplorhini.
ACKNOWLEDGMENTS
The comments of Friederun Ankel-Simons, Matt Cartmill, John Fleagle, Charlie Janson, Blythe Williams and an anonymous reviewer are greatly appreciated.
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Adaptive explanation for the origins of the anthropoidea (primates)

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