Septa and processes: convergent evolution of the orbit in haplorhine primates and strigiform birds

According to the “nocturnal visual predation hypothesis” (NVPH), the convergent eyes and orbits of primates result from selection for improved stereoscopic depth perception to facilitate manual capture of prey at night. Within primates, haplorhines share additional derived orbital morphologies, including a postorbital septum and greater orbital convergence than any other mammalian clade. While the homology and function of the haplorhine septum remain controversial, experimental data suggest that septa evolved to inhibit mechanical disturbance of the orbital contents by the anterior temporalis muscle during mastication. According to this “insulation hypothesis,” haplorhines are particularly susceptible to disruption of the orbital contents because they have large and highly convergent eyes and orbits. However, comparative tests of the insulation hypothesis have been hindered by the morphological uniqueness of the haplorhine septum among mammals. Among birds, owls (Strigiformes) exhibit an expanded postorbital process that may be functionally analogous to the haplorhine septum. Here we present a comparative analysis of orbital morphology in 103 avian species that tests two hypotheses: (1) large, convergent orbits are associated with nocturnal visual predation, and (2) the strigiform postorbital process and haplorhine postorbital septum similarly function to insulate the eyes from contractions of mandibular adductors. Strigiforms, as nocturnal visual predators, possess relatively large orbits and exhibit the highest degree of orbital convergence in our sample. Notably, orbital convergence does not scale with orbit size in birds as in mammals. Owls are also unique among the birds examined in possessing extensive, plate-like postorbital processes that largely isolate the orbits from the temporal fossae. Furthermore, dissections of four owl species demonstrate that the expanded strigiform postorbital process deflects the path of mandibular adductors around the eye's inferolateral margin. These findings provide further comparative support for both the NVPH and the insulation hypothesis.     

Muscular and osseous anatomy of the primate anterior temporal fossa and the functions of the postorbital septum

Many adaptive explanations for anthropoid origins incorporate hypotheses regarding the function of the postorbital septum. Two hypotheses are evaluated here: Cachel's ([1979b] Am. J. Phys. Anthropol. 50:1–18) hypothesis that the anthropoid postorbital septum evolved to augment muscle attachment area in the anterior temporal fossa and Cartmill's ([1980] in RL Ciochon and AB Chiarelli (eds.): Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum, pp. 243–274.) hypothesis that the septum evolved to insulate the foveate eye of haplorhines from movements in the temporal fossa during mastication. Dissections of the masticatory muscles of 55 species of primates, with emphasis on the anatomy of the anterior temporal fossa, reveal that in all anthropoids the temporal muscles take origin from the portion of the septum formed by the frontal bone. In some platyrrhines this muscle is anterior temporalis, and in others it is zygomatico-mandibularis. In tarsiers and most platyrrhines, muscle attachment to the zygomatic portion of the postorbital septum is very restricted (and of possibly varying homologies), whereas in catarrhines the zygomatico-mandibularis arises from the postorbital ridge on the zygomatic portion of the septum. This suggests that, contrary to Cachel's hypothesis, the earliest anthropoids did not have extensive areas of muscle attachment on the postorbital septum, a suggestion supported by the bony morphology of Catopithecus browni. Dissections also indicate that in all haplorhines the anteriormost temporal fibers curve around the postorbital septum between origin and insertion, implying that, were the septum not present, the anterior temporal muscles would disturb the orbital contents when contracting. This suggests that insulation may have been the septum's original function, even in the absence of a retinal fovea. In anthropoids, the rostral migration of the line of action of the anterior temporal muscles relative to the eye is attributed to their possession of extreme degrees of both orbital frontation and convergence; in tarsiers it is attributed to their possession of both massively hypertrophied eyes and moderately convergent and frontated orbits. It is argued that the postorbital septum is most likely to have evolved in a morphological context similar to that exhibited by omomyids. © 1995 Wiley-Liss, Inc.     

Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics

Hypotheses for the adaptive origin of primates have reconstructed nocturnality as the primitive activity pattern for the entire order based on functional/adaptive interpretations of the relative size and orientation of the orbits, body size and dietary reconstruction. Based on comparative data from extant taxa this reconstruction implies that basal primates were also solitary, faunivorous, and arboreal. Recently, primates have been hypothesized to be primitively diurnal, based in part on the distribution of color-sensitive photoreceptor opsin genes and active trichromatic color vision in several extant strepsirrhines, as well as anthropoid primates (Tan & Li, 1999 Nature402, 36; Li, 2000 Am. J. phys. Anthrop. Supple.30, 318). If diurnality is primitive for all primates then the functional and adaptive significance of aspects of strepsirrhine retinal morphology and other adaptations of the primate visual system such as high acuity stereopsis, have been misinterpreted for decades. This hypothesis also implies that nocturnality evolved numerous times in primates. However, the hypothesis that primates are primitively diurnal has not been analyzed in a phylogenetic context, nor have the activity patterns of several fossil primates been considered.This study investigated the evolution of activity patterns and trichromacy in primates using a new method for reconstructing activity patterns in fragmentary fossils and by reconstructing visual system character evolution at key ancestral nodes of primate higher taxa. Results support previous studies that reconstruct omomyiform primates as nocturnal. The larger body sizes of adapiform primates confound inferences regarding activity pattern evolution in this group. The hypothesis of diurnality and trichromacy as primitive for primates is not supported by the phylogenetic data. On the contrary, nocturnality and dichromatic vision are not only primitive for all primates, but also for extant strepsirrhines. Diurnality, and possibly X-linked polymorphic trichromacy, evolved at least in the stem lineage of Anthropoidea, or the stem lineage of all haplorhines.     

In vivo and in vitro bone strain in the owl monkey circumorbital region and the function of the postorbital septum

Anthropoids and tarsiers are the only vertebrates possessing a postorbital septum. This septum, formed by the frontal, alisphenoid, and zygomatic bones, separates the orbital contents from the temporal muscles. Three hypotheses suggest that the postorbital septum evolved to resist stresses acting on the skull during mastication or incision. The facial-torsion hypothesis posits that the septum resists twisting of the face about a rostrocaudal axis during unilateral mastication; the transverse-bending hypothesis argues that the septum resists caudally directed forces acting at the lateral orbital margin during mastication or incision; and the tension hypothesis suggests that the septum resists ventrally directed components of masseter muscle force during mastication and incision. This study evaluates these hypotheses using in vitro and in vivo bone strain data recorded from the circumorbital region of owl monkeys. Incisor loading of an owl monkey skull in vitro bends the face upward in the sagittal plane, compressing the interorbital region rostrocaudally and “buckling” the lateral orbital walls. Unilateral loading of the toothrow in vitro also bends the face in the sagittal plane, compressing the interorbital region rostrocaudally and buckling the working side lateral orbital wall. When the lateral orbital wall is partially cut, so as to reduce the width of its attachment to the braincase, the following changes in circumorbital bone strain patterns occur. During loading of the incisors, lower bone strain magnitudes are recorded in the interorbital region and lateral orbital walls. In contrast, during unilateral loading of the P³, higher bone strain magnitudes are observed in the interorbital region, and generally lower bone strain magnitudes are observed in the lateral orbital walls. During unilateral loading of the M², higher bone strain magnitudes are observed in both the interorbital region and in the lateral orbital wall ipsilateral to the loaded molar. Comparisons of the in vitro results with data gathered in vivo suggest that, during incision and unilateral mastication, the face is subjected to upward bending in the sagittal plane resulting in rostrocaudal compression of the interorbital region. Modeling the lateral orbital walls as curved plates suggests that during mastication the working side wall is buckled due to the dorsally directed component of the maxillary force which causes upward bending of the face in the sagittal plane. The balancing side lateral orbital wall may also be buckled due to upward bending of the face in the sagittal plane as well as being twisted by the caudoventrally directed components of the superficial masseter muscle force. The in vivo data do not exclude the possibility that the postorbital septum functions to improve the structural integrity of the postorbital bar during mastication. However, there is no reason to believe that a more robust postorbital bar could not also perform this function. Hypotheses stating that the postorbital septum originally evolved to reinforce the skull against routine masticatory loads must explain why, rather than evolving a postorbital septum, the stem anthropoids did not simply enlarge their postorbital bars. © 1996 Wiley-Liss, Inc.     

Masticatory stress, orbital orientation and the evolution of the primate postorbital bar

A postorbital bar is one of a suite of derived features which distinguishes basal primates from their putative sister taxon, plesiadapiforms. Two hypotheses have been put forward to explain postorbital bar development and variation in circumorbital form: the facial torsion model and visual predation hypothesis. To test the facial torsion model, we employ strain data on circumorbital and mandibular loading patterns in representative primates with a postorbital bar and masticatory apparatus similar to basal primates. To examine the visual predation hypothesis, we employ metric data on orbit orientation in Paleocene and Eocene primates, as well as several clades of visual predators and foragers that vary interspecifically in postorbital bar formation.A comparison of galago circumorbital and mandibular peak strains during powerful mastication demonstrates that circumorbital strains are quite low. This indicates that, as in anthropoids, the strepsirhine circumorbital region is excessively overbuilt for countering routine masticatory loads. The fact that circumorbital peak-strain levels are uniformly low in both primate suborders undermines any model which posits that masticatory stresses are determinants of circumorbital form, function and evolution. This is interpreted to mean that sufficient cortical bone must exist to prevent structural failure due to non-masticatory traumatic forces. Preliminary data also indicate that the difference between circumorbital and mandibular strains is greater in larger taxa.Comparative analyses of several extant analogs suggest that the postorbital bar apparently provides rigidity to the lateral orbital margins to ensure a high level of visual acuity during chewing and biting. The origin of the primate postorbital bar is linked to changes in orbital convergence and frontation at smaller sizes due to nocturnal visual predation and increased encephalization. By incorporating in vivo and fossil data, we reformulate the visual predation hypothesis of primate origins and thus offer new insights into major adaptive transformations in the primate skull.     

A new Middle Miocene tarsier from Thailand and the reconstruction of its orbital morphology using a geometric-morphometric method

Tarsius is an extant genus of primates endemic to the islands of Southeast Asia that is characterized by enormously enlarged orbits reflecting its nocturnal activity pattern. Tarsiers play a pivotal role in reconstructing primate phylogeny, because they appear to comprise, along with Anthropoidea, one of only two extant haplorhine clades. Their fossils are extremely rare. Here, we describe a new species of Tarsius from the Middle Miocene of Thailand. We reconstructed aspects of its orbital morphology using a geometric-morphometric method. The result shows that the new species of Tarsius had a very large orbit (falling within the range of variation of modern Tarsius) with a high degree of frontation and a low degree of convergence. Its relatively divergent lower premolar roots suggest a longer mesial tooth row and therefore a longer muzzle than in extant species. The new species documents a previous unknown Miocene group of Tarsius, indicating greater taxonomic diversity and morphological complexity during tarsier evolution. The current restriction of tarsiers to offshore islands in Southeast Asia appears to be a relatively recent phenomenon.     

Electromyography of the anterior temporalis and masseter muscles of owl monkeys (Aotus trivirgatus) and the function of the postorbital septum

Anthropoids and tarsiers are distinguished from all other vertebrates by the possession of a postorbital septum, which is formed by the frontal, alisphenoid, and zygomatic bones. Cartmill [(1980) In: Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum, p 243-274] suggested that the postorbital septum evolved in the stem lineage of tarsiers and anthropoids to insulate the eye from movements arising in the temporal fossa. Ross [(1996) Am J Phys Anthropol 91:305-324] suggested that the septum insulates the orbital contents from incursions by the line of action of the anterior temporal muscles caused by the unique combination of high degrees of orbital frontation and convergence. Both of these hypotheses must explain why insulation of the orbital contents could not be achieved by decreasing the size of the anterior temporal musculature with a corresponding increase in size of the remaining jaw adductors, rather than evolving a postorbital septum. One possibility is that the anterior temporalis is an important contributor to vertically directed bite forces during all biting and chewing activities. Another possibility is that reduction in anterior temporal musculature would compromise the ability to produce powerful bite forces, either at the incisors or along the postcanine toothrow. To evaluate these hypotheses, electromyographic (EMG) recordings were made from the masseter muscle and the anterior and posterior portions of the temporalis muscles of two owl monkeys, Aotus trivirgatus. The EMG data indicate that anterior temporalis activity relative to that of the superficial masseter is lower during incision than mastication. In addition, activity of the anterior temporalis is not consistently higher than the posterior temporalis during incision. The data indicate relatively greater activity of anterior temporalis compared to other muscles during isometric biting on the postcanine toothrow. This may be due to decreased activity in superficial masseter and posterior temporalis, rather than elevated anterior temporalis activity. The anterior temporalis is not consistently less variable in activity than the superficial masseter and posterior temporalis. The EMG data gathered here indicate no reason for suggesting that the anterior temporal muscles in anthropoids are utilized especially for incisal preparation of hard fruits. Maintenance of relatively high EMG activity in anterior temporalis across a wide range of biting behaviors is to be expected in a vertically oriented and rostrally positioned muscle such as this because, compared to the posterior temporalis, superficial masseter and medial pterygoid, it can contribute relatively larger vertical components of force to bites along the postcanine toothrow. The in vivo data do not support this hypothesis, possibly because of effects of bite point and bite force orientation.     

Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade

New crania of the Oligocene anthropoidean Aegyptopithecus provide a test of the hypothesized tarsier-anthropoidean clade. Three cranial characters shared by Tarsius and some modern anthropoideans (apical interorbital septum, postorbital septum, "perbullar" carotid pathway) were examined. 1) An apical interorbital septum is absent in Aegyptopithecus. A septum does occur in Galago senegalensis (Lorisidae) and Microcebus murinus (Cheirogaleidae), so the presence of a septum is not strong evidence favoring a tarsiiform-anthropoidean clade. 2) In Aegyptopithecus and other anthropoideans, the postorbital septum is formed mainly by a periorbital flange of the zygomatic that extends medially from the lateral orbital margin onto or near the braincase. The postorbital plate of Tarsius is formed by frontal and alisphenoid flanges that extend laterally from the braincase to the zygomatic's frontal process, which is not broader than the postorbital bars of other prosimians. Periorbital flanges evolved in Tarsius for support or protection of the enormous eyes, as suggested by the occurrence of maxillary and frontal flanges that cup portions of the eye but do not separate it from temporal muscles. 3) The internal carotid artery of Aegyptopithecus enters the bulla posteriorly and crosses the anteroventral part of the promontorium. The tympanic cavity was probably separated from the anteromedial cavity by a septum stretching from the carotid channel to the ventrolateral bullar wall. In Tarsius, the carotid pathway is prepromontorial, and a septum stretches from the carotid channel to the posteromedial bullar wall. Quantitative analyses indicate that anterior carotid position has evolved because of erect head posture. The cranium of Oligocene anthropoideans thus provides no support for the hypothesized tarsier-anthropoidean clade.     

Evolution of eye size and shape in primates

Strepsirrhine and haplorhine primates exhibit highly derived features of the visual system that distinguish them from most other mammals. Comparative data link the evolution of these visual specializations to the sequential acquisition of nocturnal visual predation in the primate stem lineage and diurnal visual predation in the anthropoid stem lineage. However, it is unclear to what extent these shifts in primate visual ecology were accompanied by changes in eye size and shape. Here we investigate the evolution of primate eye morphology using a comparative study of a large sample of mammalian eyes. Our analysis shows that primates differ from other mammals in having large eyes relative to body size and that anthropoids exhibit unusually small corneas relative to eye size and body size. The large eyes of basal primates probably evolved to improve visual acuity while maintaining high sensitivity in a nocturnal context. The reduced corneal sizes of anthropoids reflect reductions in the size of the dioptric apparatus as a means of increasing posterior nodal distance to improve visual acuity. These data support the conclusion that the origin of anthropoids was associated with a change in eye shape to improve visual acuity in the context of a diurnal predatory habitus.     

Mastication and the postorbital ligament: dynamic strain in soft tissues

Although the FEED database focuses on muscle activity patterns, it is equally suitable for other physiological recording and especially for synthesizing different types of information. The present contribution addresses the interaction between muscle activity and ligamentary stretch during mastication. The postorbital ligament is the thickened edge of a septum dividing the orbital contents from the temporal fossa and is continuous with the temporal fascia. As a tensile element, this fascial complex could support the zygomatic arch against the pull of the masseter muscle. An ossified postorbital bar has evolved repeatedly in mammals, enabling resistance to compression and shear in addition to tension. Although such ossification clearly reinforces the skull against muscle pull, the most accepted explanation is that it helps isolate the orbital contents from contractions of the temporalis muscle. However, it has never been demonstrated that the contraction of jaw muscles deforms the unossified ligament. We examined linear deformation of the postorbital ligament in minipigs, Sus scrofa, along with electromyography of the jaw muscles and an assessment of changes in pressure and shape in the temporalis. During chewing, the ligament elongated (average 0.9%, maximum 2.8%) in synchrony with the contraction of the elevator muscles of the jaw. Although the temporalis bulged outward and created substantial pressure against the braincase, the superficial fibers usually retracted caudally, away from the postorbital ligament. In anesthetized animals, stimulating either the temporalis or the masseter muscle in isolation usually elongated the ligament (average 0.4-0.7%). These results confirm that contraction of the masticatory muscles can potentially distort the orbital contents and further suggest that the postorbital ligament does function as a tension member resisting the pull of the masseter on the zygomatic arch.     

Secondarily diurnal geckos return to cost of locomotion typical of diurnal lizards

Previous studies showed that nocturnal geckos evolved a low energetic cost of locomotion (Cmin), which increases maximum aerobic speed and partially offsets the decrease in maximal oxygen consumption caused by activity at low nocturnal temperatures. Because the advantage of a low Cmin should apply at high diurnal temperatures as well as at low nocturnal temperatures, I hypothesized that Cmin remained low in geckos that have secondarily evolved diurnality. I measured Cmin in two secondarily diurnal gecko species, Rhoptropus bradfieldi (4.7 g+/-0.71 SE) and Phelsuma madagascariensis (23.9 g+/-3.7 SE), during steady exercise on a treadmill and rejected the hypothesis that secondarily diurnal geckos retain the low Cmin of their nocturnal ancestors. The Cmin in R. bradfieldi (2.468 mL O2 g-1 km-1+/-0.489 SE) and P. madagascariensis (1.389 mL O2 g-1 km-1+/-0.119 SE) returned to values typical of ancestrally diurnal lizards. This suggests that there is a trade-off that outweighs the performance advantage of low Cmin in a diurnal environment and that may cause an evolutionary association between Cmin and activity time (diurnality/nocturnality).     

Anatomical specializations for nocturnality in a critically endangered parrot, the Kakapo (Strigops habroptilus)

The shift from a diurnal to nocturnal lifestyle in vertebrates is generally associated with either enhanced visual sensitivity or a decreased reliance on vision. Within birds, most studies have focused on differences in the visual system across all birds with respect to nocturnality-diurnality. The critically endangered Kakapo (Strigops habroptilus), a parrot endemic to New Zealand, is an example of a species that has evolved a nocturnal lifestyle in an otherwise diurnal lineage, but nothing is known about its' visual system. Here, we provide a detailed morphological analysis of the orbits, brain, eye, and retina of the Kakapo and comparisons with other birds. Morphometric analyses revealed that the Kakapo's orbits are significantly more convergent than other parrots, suggesting an increased binocular overlap in the visual field. The Kakapo exhibits an eye shape that is consistent with other nocturnal birds, including owls and nightjars, but is also within the range of the diurnal parrots. With respect to the brain, the Kakapo has a significantly smaller optic nerve and tectofugal visual pathway. Specifically, the optic tectum, nucleus rotundus and entopallium were significantly reduced in relative size compared to other parrots. There was no apparent reduction to the thalamofugal visual pathway. Finally, the retinal morphology of the Kakapo is similar to that of both diurnal and nocturnal birds, suggesting a retina that is specialised for a crepuscular niche. Overall, this suggests that the Kakapo has enhanced light sensitivity, poor visual acuity and a larger binocular field than other parrots. We conclude that the Kakapo possesses a visual system unlike that of either strictly nocturnal or diurnal birds and therefore does not adhere to the traditional view of the evolution of nocturnality in birds.     

Influence of Orbit Size on Aspects of the Tarsier Postorbital Septum

Explanations invoking the complex mechanical effects of orbital enlargement in Tarsius have been extended to several areas of the skull, including the conformation of the postorbital septum. The strong cline in the degree of relative orbital enlargement across tarsier species groups presents an unexploited opportunity to test such scenarios. Our goal is to evaluate hypotheses concerning the impact of orbital hypertrophy on the size of specific components of the postorbital region including the frontal, zygomatic, alisphenoid, and maxillary bones. The frontal process is almost always viewed as a functional projection whose bracing role requires a positive morphometric association with orbital hypertrophy. Conversely, the periorbital expansion of the zygomatic is often perceived as functionally unrelated to orbital enlargement and therefore is not expected to track increases in relative orbit size. Interpretations of the alisphenoid and maxillary periorbital processes range from vestigial remnants of once larger structures reduced because of ocular enlargement to structures large in tarsiers because of their functionally relevant role in supporting the enlarged ocular apparatus. We measured these attributes in an extensive sample of 4 tarsier species groups including Tarsius bancanus, T. syrichta, T. spectrum, and T. pumilus. In contrast to proposed functional interpretations, our results indicate that variation in most linear parameters might be better explained by differences in body size than intrageneric differences in orbit size. As expected, width of the zygomatic postorbital contribution does not parallel intrageneric variation in orbit size. However, morphometric relationships between relative orbit size and other parts of the septum are complex but not clearly associated with orbit size differences within Tarsius.     

Effects of activity pattern on eye size and orbital aperture size in primates

Among primates, nocturnal species exhibit relatively larger orbital apertures than diurnal species. Most researchers have considered this disparity in orbital aperture size to reflect differences in eye size, with nocturnal primates having relatively large eyes in order to maximize visual sensitivity. Presumed changes in eye size due to shifts in activity pattern are an integral part of theoretical explanations for many derived features of anthropoids, including highly convergent orbits and a postorbital septum. Here I show that despite clear differences in relative orbital aperture size, many diurnal and nocturnal primates do not differ in relative eye size. Among nocturnal primates, relative eye size is influenced by diet. Nocturnal visual predators (e.g., Tarsius, Loris, and Galago moholi) tend to have larger relative eye sizes than diurnal primates. By contrast, nocturnal frugivores (e.g., Perodicticus, Nycticebus, and Cheirogaleus) have relative eye sizes that are comparable to those of diurnal primates. Although some variation in orbital aperture size can be attributed to variation in eye size, both cornea size and orbit orientation also exert a strong influence on orbital aperture size. These findings argue for caution in the use of relative orbital aperture size as an indicator of activity pattern in fossil primates. These findings further suggest that existing scenarios for the evolution of unique orbital morphologies in anthropoids must be modified to reflect the importance of ecological variables other than activity pattern.     

A paleoecological model for the origin of higher primates

Tertiary climatic oscillations initiated the origin of anthropoid primates. A paleoecological model of anthropoid evolution is presented which assumes increasing global seasonality in the late Eocene. Size changes are effected to stabilize internal temperature fluctuations under cooler climatic conditions. Because larger body size is associated with diurnality and reduced litter size, these anthropoid behavoral and reproductive features also fit into the model. Dietary changes involving an emphasis on frugivory, which becomes a more predictable dietary mode under seasonal conditions, can be associated with the development of a post-orbital septum, a broad mesiodistal incisal span, the evolution of color vision, reduction of the olfactory bulbs, and the concomitant enlargement of areas of the brain relating to the processing of visual information. Finally, postural behavior or locomotion might be included in this model if frugivorous foraging and feeding behavior led to the development of a basic level of anthropoid locomotor morphology, involving adaptations for arboreal quadrupedalism.     

Biophysical modeling of the temporal niche: from first principles to the evolution of activity patterns

Most mammals can be characterized as nocturnal or diurnal. However infrequently, species may overcome evolutionary constraints and alter their activity patterns. We modeled the fundamental temporal niche of a diurnal desert rodent, the golden spiny mouse, Acomys russatus. This species can shift into nocturnal activity in the absence of its congener, the common spiny mouse, Acomys cahirinus, suggesting that it was competitively driven into diurnality and that this shift in a small desert rodent may involve physiological costs. Therefore, we compared metabolic costs of diurnal versus nocturnal activity using a biophysical model to evaluate the preferred temporal niche of this species. The model predicted that energy expenditure during foraging is almost always lower during the day except during midday in summer at the less sheltered microhabitat. We also found that a shift in summer to foraging in less sheltered microhabitats in response to predation pressure and food availability involves a significant physiological cost moderated by midday reduction in activity. Thus, adaptation to diurnality may reflect the "ghost of competition past"; climate-driven diurnality is an alternative but less likely hypothesis. While climate is considered to play a major role in the physiology and evolution of mammals, this is the first study to model its potential to affect the evolution of activity patterns of mammals.     

Function of the mammalian postorbital bar

Complete postorbital bars, bony arches that encompass the lateral aspect of the eye and form part of a circular orbit, have evolved homoplastically multiple times during mammalian evolution. Numerous functional hypotheses have been advanced for postorbital bars, the most promising being that postorbital bars function to stiffen the lateral orbit in taxa that have significant angular deviation between the temporal fossa and the bony orbit. Without a stiff lateral orbit the anterior temporalis muscle and fascia potentially would pull on the postorbital ligament, deform the orbit, and cause disruption of oculomotor precision. Morphometric data were collected on 1,329 specimens of 324 taxa from 16 orders of extant eutherian and metatherian mammals in order to test whether the orientation of the orbit relative to the temporal fossa is correlated with the replacement of the postorbital ligament with bone. The allometric and ecological influences on orbit orientation across mammals are also explored. The morphometric results corroborate the hypothesis: Shifts in orbit orientation relative to the temporal fossa are correlated with the size of the postorbital processes, which replace the ligament. The allometric and ecological factors that influence orbit orientation vary across taxa. Postorbital bars stiffen the lateral orbital wall. Muscle pulleys, ligaments, and other connective tissue attach to the lateral orbital wall, including the postorbital bar. Without a stiff lateral orbit, deformation due to temporalis contraction would displace soft tissues contributing to normal oculomotor function.     

Protoanthropoidea (Primates, Simiiformes): A New Primate Higher Taxon and a Solution to the Rooneyia Problem

As a derivative of the hypothesis that anthropoids evolved from omomyid-like primates, the enigmatic North American fossil Rooneyia viejaensis, from the latest Eocene of Texas, is placed in a new higher taxon, Protoanthropoidea, which is proposed as the sister-group of Anthropoidea. Rooneyia and anthropoids share synapomorphically a pattern of character states relating to the unique orbital morphology of higher primates, including; highly convergent and frontated orbits roofed above by an extended frontal bone; funnel-shaped orbital fossae; orbital apices that are recessed beneath the forebrain; a deep, large lateral process of the frontal bone (upper portion of the postorbital bar) that may presage closure of the orbit by an enlarged ascending process of the zygomatic. If the sister-group of anthropoids occupied North America as part of a Laurasian geographic distribution during the Paleogene, as some primate genera did, ancestral anthropoids may likewise have occurred across Laurasia, prestaging them to enter Africa and Central/South America in two independent episodes of dispersal—without having the ancestral platyrrhines crossing the daunting Atlantic Ocean.     

Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology.

Linear dimensions and angular orientations of the browridge, postorbital bar, and postorbital septum were obtained from a representative series of primates and compared with variables associated with several nonmechanical and biomechanical/mechanical models put forward to explain the form and function of the circumorbital region. Analyses of the results indicate that face size is the primary determinant of variation in primate circumorbital morphology. Anteroposterior browridge thickness is correlated with neural-orbital disjunction among anthropoid primates, but not among prosimians. This difference appears related to differences in the construction of the upper face and anterior cranial fossa between prosimians and anthropoids. Little support is demonstrated for the anterior dental loading model of browridge development. Mediolateral postorbital bar width and (to a lesser degree) browridge height are correlated with neurofacial torsion during mastication and variation in masticatory muscle size. These analyses further suggest that since circumorbital structures (especially the browridges) are located the farthest away from the chewing apparatus, they are least affected by masticatory stresses.     

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyper-enlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal–diurnal dichotomy that has long informed debate on the origin of anthropoid primates.