E. Christopher Kirk

Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set.

We present a compilation of endocranial volumes (ECV) for 176 non-human primate species based on individual data collected from 3813 museum specimens, at least 88% being wild-caught. In combination with body mass data from wild individuals, strong correlations between endocranial volume and body mass within taxonomic groups were found. Errors attributable to different techniques for measuring cranial capacity were negligible and unbiased. The overall slopes for regressions of log ECV on log body mass in primates are 0.773 for least-squares regression and 0.793 for reduced major axis regression. The least-squares slope is reduced to 0.565 when independent contrasts are substituted for species means (branch lengths from molecular studies). A common slope of 0.646 is obtained with logged species means when grade shifts between major groups are taken into account using ANCOVA. In addition to providing a comprehensive and reliable database for comparative analyses of primate brain size, we show that the scaling relationship between brain mass and ECV does not differ significantly from isometry in primates. We also demonstrate that ECV does not differ substantially between captive and wild samples of the same species. ECV may be a more reliable indicator of brain size than brain mass, because considerably larger samples can be collected to better represent the full range of intraspecific variation. We also provide support for the maternal energy hypothesis by showing that basal metabolic rate (BMR) and gestation period are both positively correlated with brain size in primates, after controlling for the influence of body mass and potential effects of phylogenetic relatedness.

Osteological evidence for the evolution of activity pattern and visual acuity in primates

Examination of orbit size and optic foramen size in living primates reveals two adaptive phenomena. First, as noted by many authors, orbit size is strongly correlated with activity pattern. Comparisons of large samples of extant primates consistently reveal that nocturnal species exhibit proportionately larger orbits than diurnal species. Furthermore, nocturnal haplorhines (Tarsius and Aotus) have considerably larger orbits than similar-sized nocturnal strepsirrhines. Orbital hypertrophy in Tarsius and Aotus accommodates the enormously enlarged eyes of these taxa. This extreme ocular hypertrophy seen in extant nocturnal haplorhines is an adaptation for both enhanced visual acuity and sensitivity in conditions of low light intensity. Second, the relative size of the optic foramen is highly correlated with the degree of retinal summation and inferred visual acuity. Diurnal haplorhines exhibit proportionately larger optic foramina, less central retinal summation, and much higher visual acuity than do all other primates. Diurnal strepsirrhines exhibit a more subtle but significant parallel enlargement of the optic foramen and a decrease in retinal summation relative to the condition seen in nocturnal primates. These twin osteological variables of orbit size and optic foramen size may be used to draw inferences regarding the activity pattern, retinal anatomy, and visual acuity of fossil primates. Our measurements demonstrate that the omomyiforms Microchoerus, Necrolemur, Shoshonius, and Tetonius, adapiform Pronycticebus, and the possible lorisiform Plesiopithecus were likely nocturnal on the basis of orbit diameter. The adapiforms Leptadapis, Adapis, and Notharctus, the phylogenetically enigmatic Rooneyia, the early anthropoids Proteopithecus, Catopithecus, and Aegyptopithecus, and early platyrrhine Dolichocebus were likely diurnal. The activity pattern of the platyrrhine Tremacebus is obscure. Plesiopithecus, Pronycticebus, Microchoerus, and Necrolemur probably had eyes that were very similar to those of extant nocturnal primates, with a high degree of retinal summation and rod-dominated retinae. Leptadapis and Rooneyia likely had eyes similar to those of extant diurnal strepsirrhines, with moderate degrees of retinal summation, a larger cone:rod ratio than in nocturnal primates, and, more speculatively, well-developed areae centrales similar to those of diurnal strepsirrhines. Adapis exhibited uncharacteristically high degrees of retinal summation for a small-eyed (likely diurnal) primate. None of the adapiform or omomyiform taxa for which we were able to obtain optic foramen dimensions exhibited the extremely high visual acuity characteristic of extant diurnal haplorhines.

The Evolution of High Visual Acuity in the Anthropoidea

Most definitions of the order primates make some reference to the importance of vision relative to the other special senses (Le Gros Clark, 1959; Martin, 1990; Napier and Napier, 1967). This characterization is particularly fitting for haplorhine primates, in which vision is unquestionably the dominant sensory modality. Anthropoids and tarsiers differ from strepsirrhines in exhibiting a derived reduction of the olfactory apparatus (Baron et al., 1983; Cave, 1973) and an elaboration of the visual sense to a degree that is unique among mammals (Rodieck, 1973; Walls, 1942). Visual adaptations, however, are divergent within the haplorhine suborder. While the tarsier visual system is primarily specialized for enhanced sensitivity in the context of nocturnal visual predation (Castenholz, 1984s), most living anthropoids are adapted for extremely acute diurnal vision.

Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms.

Arboreal primates have distinctive intrinsic hand proportions compared with many other mammals. Within Euarchonta, platyrrhines and strepsirrhines have longer manual proximal phalanges relative to metacarpal length than colugos and terrestrial tree shrews. This trait is part of a complex of features allowing primates to grasp small-diameter arboreal substrates. In addition to many living and Eocene primates, relative elongation of proximal manual phalanges is also present in most plesiadapiforms. In order to evaluate the functional and evolutionary implications of manual similarities between crown primates and plesiadapiforms, we measured the lengths of the metacarpal, proximal phalanx, and intermediate phalanx of manual ray III for 132 extant mammal species (n=702 individuals). These data were compared with measurements of hands in six plesiadapiform species using ternary diagrams and phalangeal indices. Our analyses reveal that many arboreal mammals (including some tree shrews, rodents, marsupials, and carnivorans) have manual ray III proportions similar to those of various arboreal primates. By contrast, terrestrial tree shrews have hand proportions most similar to those of other terrestrial mammals, and colugos are highly derived in having relatively long intermediate phalanges. Phalangeal indices of arboreal species are significantly greater than those of the terrestrial species in our sample, reflecting the utility of having relatively long digits in an arboreal context. Although mammals known to be capable of prehensile grips demonstrate long digits relative to palm length, this feature is not uniquely associated with manual prehension and should be interpreted with caution in fossil taxa. Among plesiadapiforms, Carpolestes, Nannodectes, Ignacius, and Dryomomys have manual ray III proportions that are unlike those of most terrestrial species and most similar to those of various arboreal species of primates, tree shrews, and rodents. Within Euarchonta, Ignacius and Carpolestes have intrinsic hand proportions most comparable to those of living arboreal primates, while Nannodectes is very similar to the arboreal tree shrew Tupaia minor. These results provide additional evidence that plesiadapiforms were arboreal and support the hypothesis that Euarchonta originated in an arboreal milieu.

New perspectives on anthropoid origins.

Adaptive shifts associated with human origins are brought to light as we examine the human fossil record and study our own genome and that of our closest ape relatives. However, the more ancient roots of many human characteristics are revealed through the study of a broader array of living anthropoids and the increasingly dense fossil record of the earliest anthropoid radiations. Genomic data and fossils of early primates in Asia and Africa clarify relationships among the major clades of primates. Progress in comparative anatomy, genomics, and molecular biology point to key changes in sensory ecology and brain organization that ultimately set the stage for the emergence of the human lineage.

Protection from Acoustic Trauma Is Not a Primary Function of the Medial Olivocochlear Efferent System

The medial olivocochlear (MOC) efferent system is an important component of an active mechanical outer hair cell system in mammals. An extensive neurophysiological literature demonstrates that the MOC system attenuates the response of the cochlea to sound by reducing the gain of the outer hair cell mechanical response to stimulation. Despite a growing understanding of MOC physiology, the biological role of the MOC system in mammalian audition remains uncertain. Some evidence suggests that the MOC system functions in a protective role by acting to reduce receptor damage during intense acoustic exposure. For the MOC system to have evolved as a protective mechanism, however, the inner ears of mammals must be exposed to potentially damaging sources of noise that can elicit MOC-mediated protective effects under natural conditions. In this review, we evaluate the possibility that the MOC system evolved to protect the inner ear from naturally occurring environmental noise. Our survey of nonanthropogenic noise levels shows that while sustained sources of broadband noise are found in nearly all natural acoustic environments, frequency-averaged ambient noise levels in these environments rarely exceed 70 dB SPL. Similarly, sources reporting ambient noise spectra in natural acoustic environments suggest that noise levels within narrow frequency bands are typically low in intensity (<40 dB SPL). Only in rare instances (e.g., during frog choruses) are ambient noise levels sustained at moderately high intensities (~70–90 dB SPL). By contrast, all experiments in which an MOC-mediated protective effect was demonstrated used much higher sound intensities to traumatize the cochlea (100–150 dB SPL). This substantial difference between natural ambient noise levels and the experimental conditions necessary to evoke MOC-mediated protection suggests that even the noisiest natural acoustic environments are not sufficiently intense to have selected for the evolution of the MOC system as a protective mechanism. Furthermore, although relatively intense noise environments do exist in nature, they are insufficiently distributed to account for the widespread distribution of the MOC system in mammals. The paucity of high-intensity noise and the near ubiquity of low-level noise in natural environments supports the hypothesis that the MOC system evolved as a mechanism for “unmasking” biologically significant acoustic stimuli by reducing the response of the cochlea to simultaneous low-level noise. This suggested role enjoys widespread experimental support.

Eye Morphology in Cathemeral Lemurids and Other Mammals

The visual systems of cathemeral mammals are subject to selection pressures that are not encountered by strictly diurnal or nocturnal species. In particular, the cathemeral eye and retina must be able to function effectively across a broad range of ambient light intensities. This paper provides a review of the current state of knowledge regarding the visual anatomy of cathemeral primates, and presents an analysis of the influence of cathemerality on eye morphology in the genus Eulemur. Due to the mutual antagonism between most adaptations for increased visual acuity and sensitivity, cathemeral lemurs are expected to resemble other cathemeral mammals in having eye morphologies that are intermediate between those of diurnal and nocturnal close relatives. However, if lemurs only recently adopted cathemeral activity patterns, then cathemeral lemurids would be expected to demonstrate eye morphologies more comparable to those of nocturnal strepsirrhines. Both predictions were tested through a comparative study of relative cornea size in mammals. Intact eyes were collected from 147 specimens of 55 primate species, and relative corneal dimensions were compared to measurements taken from a large sample of non-primate mammals. These data reveal that the five extant species of the cathemeral genus Eulemur have relative cornea sizes intermediate between those of diurnal and nocturnal strepsirrhines. Moreover, all Eulemur species have relative cornea sizes that are comparable to those of cathemeral non-primate mammals and significantly smaller than those of nocturnal mammals. These results suggest that Eulemur species resemble other cathemeral mammals in having eyes that are adapted to function under variable environmental light levels. These results also suggest that cathemerality is a relatively ancient adaptation in Eulemur that was present in the last common ancestor of the genus (ca. 8–12 MYA).

Eye shape and the nocturnal bottleneck of mammals

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. By contrast, several studies have concluded that many mammals exhibit typical nocturnal eye shapes, regardless of activity pattern. However, a recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night). Here, we conduct a detailed analysis of eye shape and activity pattern in mammals, using a broad comparative sample of 266 species. We find that the eye shapes of cathemeral mammals completely overlap with nocturnal and diurnal species. Additionally, most diurnal and cathemeral mammals have eye shapes that are most similar to those of nocturnal birds and lizards. The only mammalian clade that diverges from this pattern is anthropoids, which have convergently evolved eye shapes similar to those of diurnal birds and lizards. Our results provide additional evidence for a nocturnal ‘bottleneck’ in the early evolution of crown mammals.

Cochlear labyrinth volume and hearing abilities in primates.

The primate cochlea is a membranous, fluid‐filled receptor organ that is specialized for sound detection. Like other parts of the inner ear, the cochlea is contained within the bony labyrinth of the petrous temporal bone. The close anatomical relationship between the bony cochlear labyrinth and the membranous cochlea provides an opportunity to quantify cochlear size using osteological specimens. Although mechanisms of cochlear frequency analysis are well studied, relatively little is known about the functional consequences of interspecific variation in cochlear size. Previous comparative analyses have linked increases in basilar membrane length to decreases in both the high and low frequency limits of hearing in mammals. However, these analyses did not consider the potentially confounding effects of body mass or phylogeny. Here, we present measurements of cochlear labyrinth volume in 33 primate species based on high‐resolution computed tomography. These data demonstrate that cochlear labyrinth volume is strongly negatively allometric with respect to body mass. Scaling of cochlear volume in primates is very similar to scaling of basilar membrane length among mammals generally. Furthermore, an analysis of 10 primate taxa with published audiograms reveals that cochlear labyrinth volume is significantly negatively correlated with the high frequency limit of hearing. This result is independent of body mass and phylogeny, suggesting that cochlear size is functionally related to the range of audible frequencies in primates. Although the nature of this functional relationship remains speculative, our findings suggest that some hearing parameters of extinct taxa may be estimated using fossil petrosals. Anat Rec, 292:765–776, 2009.

First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism

Previously known only from isolated teeth and lower jaw fragments recovered from the Cretaceous and Palaeogene of the Southern Hemisphere, the Gondwanatheria constitute the most poorly known of all major mammaliaform radiations. Here we report the discovery of the first skull material of a gondwanatherian, a complete and well-preserved cranium from Upper Cretaceous strata in Madagascar that we assign to a new genus and species. Phylogenetic analysis strongly supports its placement within Gondwanatheria, which are recognized as monophyletic and closely related to multituberculates, an evolutionarily successful clade of Mesozoic mammals known almost exclusively from the Northern Hemisphere. The new taxon is the largest known mammaliaform from the Mesozoic of Gondwana. Its craniofacial anatomy reveals that it was herbivorous, large-eyed and agile, with well-developed high-frequency hearing and a keen sense of smell. The cranium exhibits a mosaic of primitive and derived features, the disparity of which is extreme and probably reflective of a long evolutionary history in geographic isolation.