Diet drove brain and dental morphological coevolution in strepsirrhine primates.

The evolution of the remarkably complex primate brain has been a topic of great interest for decades. Multiple factors have been proposed to explain the comparatively larger primate brain (relative to body mass), with recent studies indicating diet has the greatest explanatory power. Dietary specialisations also correlate with dental adaptations, providing a potential evolutionary link between brain and dental morphological evolution. However, unambiguous evidence of association between brain and dental phenotypes in primates remains elusive. Here we investigate the effect of diet on variation in primate brain and dental morphology and test whether the two anatomical systems coevolved. We focused on the primate suborder Strepsirrhini, a living primate group that occupies a very wide range of dietary niches. By making use of both geometric morphometrics and dental topographic analysis, we extend the study of brain-dental ecomorphological evolution beyond measures of size. After controlling for allometry and evolutionary relatedness, differences in brain and dental morphology were found between dietary groups, and brain and dental morphologies were found to covary. Historical trajectories of morphological diversification revealed a strong integration in the rates of brain and dental evolution and similarities in their modes of evolution. Combined, our results reveal an interplay between brain and dental ecomorphological adaptations throughout strepsirrhine evolution that can be linked to diet.

The role of developmental rate, body size, and positional behavior in the evolution of covariation and evolvability in the cranium of strepsirrhines and catarrhines.

Recent studies on hominin craniofacial evolution have focused on phenotypic integration or covariation among traits. Covariation is thought to significantly affect evolutionary trajectories, shaping the ways in which hominins and other primates could have evolved. However, the ways in which covariation itself evolves are not well understood. This study aims to investigate the role of phylogeny, development, body size, and positional behavior in shaping the strength of covariation in strepsirrhine and catarrhine primate crania (n = 1009, representing 11 genera). These factors may have been catalysts for change in the magnitude of covariation, and they have changed significantly during primate evolution and particularly hominin evolution. Modern humans in particular have slow developmental trajectories, large bodies, and a unique form of locomotion in the form of orthograde bipedalism. Variance of eigenvalues, mean integration, mean evolvability, and mean conditional evolvability was estimated and their relationship to the various factors described earlier was assessed using phylogenetic and nonphylogenetic analyses. Results indicate that some phylogenetic signal is present, but it is not equivalent across integration statistics or cranial regions. In particular, these results suggest that closely related species are more similar than more distantly related species in evolvability of the cranial base and integration of the face. Two divergent patterns were also identified, in which covariation and evolvability of the cranial base are linked to developmental rate, but those of the face are linked to body size. Neither locomotion nor posture appears related to covariation or evolvability of the primate cranium. These results suggest that overall low covariation observed in the hominin cranium may be a result of separate trends in different cranial regions.

The evolution of palate shape in the Lepilemur-Cheirogaleidae clade (Primates: Strepsirrhini).

OBJECTIVES: Phylogenies consistently group the folivorous Lepilemur species with the small-bodied insectivorous-frugivorous cheirogaleids. Juvenile lepilemurs and adult cheirogaleids share allometries in most aspects of skull morphology, except the palate. We investigated potential influences on palate shape in these taxa and several outgroups using geometric morphometrics. MATERIALS AND METHODS: Our sample included representatives of four extant strepsirrhine families, Cheirogaleidae (including Lepilemurinae), Lemuridae, Indriidae, and Galagidae, and one subfossil Megaladapis. Our dataset comprised 32 landmarks collected from 397 specimens representing 15 genera and 28 species, and was analyzed using generalized procrustes analyses and between group principal component analysis. We explored the influence of size, phylogeny, diet, and the propagation of loud vocalizations on palate shape. RESULTS: While congeneric species clustered within the morphospace, the phylomorphospace did not mirror molecular phylogenetic hypotheses of higher-order relationships. Four palate forms were distinguished within the Cheirogaleidae. Diet, strongly linked to body size, had the single greatest influence on palate shape. The production of long-distance advertisement calls was most often associated with positive scores on the PC1 axis. DISCUSSION: Our results suggest that the extensive variation in palate shape among Cheirogaleidae is related to dietary shifts that accompanied changes in body size during the clade's radiation. Molecular phylogenies indicate that cheirogaleid diversification involved repeated dwarfing events, which in turn drove dietary shifts from ancestral folivory-frugivory to frugivory, gummivory, and faunivory in the descendant species. The elongated Lepilemur palate is probably related to accelerated eruption of the cheek teeth to render juveniles competent to shear leaves upon weaning.

First navicular remains of a European adapiform (Anchomomys frontanyensis) from the Middle Eocene of the Eastern Pyrenees (Catalonia, Spain): implications for early primate locomotor behavior and navicular evolution.

We describe the first known navicular bones for an Eocene euprimate from Europe and assess their implications for early patterns of locomotor evolution in primates. Recovered from the fossil site of Sant Jaume de Frontanyà-3C (Barcelona, Spain), the naviculars are attributed to Anchomomys frontanyensis. The small size of A. frontanyensis allows us to consider behavioral implications of comparisons with omomyiforms, regardless of allometric sources of navicular variation. Researchers usually consider omomyiforms to be more prone to leaping than contemporaneous adapiforms partly because of the more pronounced elongation of omomyiform tarsal elements. However, A. frontanyensis differs from other adapiforms and is similar to some omomyiforms in its more elongated navicular proportions. Although this might raise questions about attribution of these naviculars to A. frontanyensis, the elements exhibit clear strepsirrhine affinities leaving little doubt about the attribution: the bones' mesocuneiform facets contact their cuboid facets. We further propose that this strepsirrhine-specific feature in A. frontanyensis and other adapiforms reflects use of more inverted foot postures and potentially smaller substrates than sympatric omomyiforms that lack it. Thus substrate differences may have influenced niche partitioning in Eocene euprimate communities along with differences in locomotor agility. As previous studies on the astragalus and the calcaneus have suggested, this study on the navicular is consistent with the hypothesis that the locomotor mode of A. frontanyensis was similar to that of extant cheirogaleids, especially species of Microcebus and Mirza.

A primate with a Panda's thumb: The anatomy of the pseudothumb of Daubentonia madagascariensis.

OBJECTIVES: Accessory digits have evolved independently within several mammalian lineages. Most notable among these is the pseudothumb of the giant panda, which has long been considered one of the most extraordinary examples of contingent evolution. To date, no primate has been documented to possess such an adaptation. Here, we investigate the presence of this structure within the aye-aye (Daubentonia madagascariensis), a species renowned for several other specialized morphological adaptations in the hand, including a morphologically unique third digit. MATERIALS AND METHODS: We combine physical dissection techniques with digital imaging processes across a sample of seven individuals (six adults and one immature individual) to describe and visualize the anatomy of the wrist and hand within the aye-aye. RESULTS: A distinct pseudothumb, which consists of both a bony component (an expanded radial sesamoid) and a dense cartilaginous extension (the "prepollex") was observed in all specimens. We demonstrate that this pseudodigit receives muscular attachments from three muscles, which collectively have the potential to enable abduction, adduction, and opposition. Finally, we demonstrate that the pseudothumb possesses its own distinct pad within the palm, complete with independent dermatoglyphs. DISCUSSION: Pseudothumbs have been suggested to improve palmar dexterity in taxa with overly -generalized first digits (e.g., pandas) and to widen the hand for digging (e.g., some fossorial moles), but the aye-aye's pseudothumb represents what we believe is a heretofore unrecognized third functional role: its accessory digit compensates for overspecialization of its fingers for non-gripping functions (in this case, the aye-aye's unique "tap foraging" practices).

DiceCT Analysis of the Extreme Gouging Adaptations Within the Masticatory Apparatus of the Aye-Aye (Daubentonia madagascariensis).

Relative to all other primates, the aye-aye (Daubentonia madagascariensis) exists at the extremes of both morphology and behavior. Its specialized anatomy-which includes hypselodont incisors and highly derived manual digits-reflects a dietary niche, unique among primates, which combines tap-foraging with gouging to locate and extract wood-boring larvae. Here, we explore the impact of this extreme dietary ecology upon the masticatory musculature of this taxon with reference to a second, similarly sized but highly generalist lemuriform-the mongoose lemur (Eulemur mongoz). Using non-destructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography techniques, we reconstruct the three-dimensional volumes of eight masticatory muscles, and, for the first time in strepsirrhines, isolate and visualize their constituent muscle fascicles in situ and in three dimensions. Using these data, we report muscle volumes, forces, and fascicle lengths from each muscle portion, as well as their orientation relative to two standardized anatomical planes. Our findings demonstrate the overbuilt nature of the aye-aye's masticatory apparatus, in which each muscle possesses an absolutely and relatively larger muscle volume and PCSA than its counterpart in the mongoose lemur. Likewise, for several adductor muscles, aye-ayes also possess relatively greater fascicle lengths. Finally, we note several unusual features within the lateral pterygoid of the aye-aye-the muscle most responsible for jaw protrusion-that relate to force maximization and reorientation. As this jaw motion is critical to gouging, we interpret these differences to reflect highly specific specializations that facilitate the aye-aye's extreme subsistence strategy. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:282-294, 2020. © 2019 American Association for Anatomy.

A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center.

Scientific study of lemurs, a group of primates found only on Madagascar, is crucial for understanding primate evolution. Unfortunately, lemurs are among the most endangered animals in the world, so there is a strong impetus to maximize as much scientific data as possible from available physical specimens. MicroCT scanning efforts at Duke University have resulted in scans of more than 100 strepsirrhine cadavers representing 18 species from the Duke Lemur Center. An error study of the microCT scanner recovered less than 0.3% error at multiple resolution levels. Scans include specimen overviews and focused, high-resolution selections of complex anatomical regions (e.g., cranium, hands, feet). Scans have been uploaded to MorphoSource, an online digital repository for 3D data. As captive (but free ranging) individuals, these specimens have a wealth of associated information that is largely unavailable for wild populations, including detailed life history data. This digital collection maximizes the information obtained from rare and endangered animals with minimal degradation of the original specimens.

A comparison of relief estimates used in three-dimensional dental topography.

OBJECTIVES: Topographic estimates of dental relief are now commonly used to make dietary inferences from the teeth of extant and extinct primates. We thoroughly compared commonly used relief estimates in an effort to help researchers decide which variable best suits their objectives. MATERIALS AND METHODS: We combined a total of three datasets: five theoretical models built to compare the effect of tooth complexity and basin depth on relief estimates, a dataset of 110 lower molars of prosimians, and a dataset of 25 upper molars of apes. We investigated intra-mesh variation and tooth average relief, estimated from slope and three different relief indices, according to four criteria: (1) the ability to map relief on topographic maps, (2) the correlation with other relief estimates, (3) the ability to separate high-relief molars of folivores from deep-relief molars of insectivores in prosimians, and (4) the influence of surface complexity on relief estimates in apes. RESULTS: We found that polygon slope and relief index are linked by a mathematical relation. Tooth average slope and all relief indices are strongly correlated. In contrast, relief estimates are moderately correlated to cusp elevation. One relief index of four relief estimates had an excellent ability to separate high-relief from deep-relief molars in prosimians, whereas slope could not separate them. No significant effect of tooth complexity on dental relief could be detected in apes. CONCLUSIONS: Because slope and relief indices are highly correlated, it is strongly recommended not to combine them in multivariate analysis. Still, slope and relief indices show interesting differences in scaling, graphical representation, computation method, and ability to separate high-relief and deep-relief molars. Our results also suggest that slope and relief indices can vary independently of tooth complexity and are moderately affected by mean cusp elevation in apes.

Middle ear pneumatization in nonhuman primates: A comparative analysis.

OBJECTIVES: We test the effects of body mass and phylogeny on middle ear cavity pneumatization, and the role of pneumatization in hearing function, spanning the anatomical, ecological, and behavioral diversity of nonhuman primates. MATERIALS AND METHODS: All cavities were segmented in middle ear scans of 96 specimens, from 12 strepsirrhine and 15 haplorhine extant species. We measured the tympanic cavity (TC) separately, and all other middle ear spaces together (MES), calculating the degree of pneumatization with the surface area-to-volume ratio. We tested body mass effect with linear regression; we evaluated the phylogenetic signal and selection patterns, using a Kappa statistic test, and Ornstein-Uhlenbeck models (OU). We investigated the link between pneumatization and hearing sensitivity using phylogenetic regression. RESULTS: Testing body mass reveals an allometric pattern for both TC and MES dimensions. Degree of pneumatization in MES is dependent on body mass in haplorhines: larger animals have more pneumatized MES. Differences at various taxonomic ranks were observed for MES, while no phylogenetic influence was observed for TC. Infraorder selection patterns are different. Auditory performance is significantly related to degree of pneumatization, indicating that a pneumatized middle ear is associated with better perception of low frequencies. DISCUSSION: Pneumatization in MES is under differential selective pressure, indicating several optima for this trait. Pneumatization in MES probably modifies hearing sensitivity through pressure regulation mechanisms, auditory bulla size reduction, and frequency modulation. This could explain strepsirrhine adaptation to high-frequency perception, while haplorhine auditory perception is adapted to a broader sound range, including high and low frequencies.

Ambient occlusion and PCV (portion de ciel visible): A new dental topographic metric and proxy of morphological wear resistance.

Recently, ambient occlusion, quantified through portion de ciel visible (PCV) was introduced as a method for quantifying dental morphological wear resistance and reconstructing diet in mammals. Despite being used to reconstruct diet and investigate the relationship between dental form and function, no rigorous analysis has investigated the correlation between PCV and diet. Using a sample of platyrrhine and prosimians M2s, we show average PCV was significantly different between most dietary groups. In prosimian, insectivores had the lowest PCV, followed by folivores, omnivores, frugivores, and finally hard-object feeders. In platyrrhines, omnivores had the lowest average PCV, followed by folivores, frugivores, and finally hard-object feeders. PCV was correlated to two topographic variables (Dirichlet normal energy, DNE, and relief index, RFI) but uncorrelated to three others (orientation patch count rotated, OPCR, tooth surface area, and tooth size). The OPCR values here differed greatly from previously published values using the same sample, showing how differences in data acquisition (i.e., using 2.5D vs. 3D surfaces) can lead to drastic differences in results. Compared to other popular topographic variables, PCV performed as well or better at predicting diet in these groups, and when combined with a metric for size, the percent of successful dietary classifications reached 90%. Further, using an ontogenetic series of hominin (Paranthropus robustus) M2s, we show that PCV correlates well with probability of wear, with PCV values being higher on the portions of the occlusal surface that experience more wear (e.g., cusps and crest tips, wear facets) than the portions of the tooth that experience less. This relationship is strongest once wear facets have begun to form on the occlusal surface. These results highlight the usefulness of PCV in quantifying morphological wear resistance and predicting diet in mammals.

Convergent evolution in the Euarchontoglires.

Convergence-the independent evolution of similar phenotypes in distantly related clades-is a widespread and much-studied phenomenon. An often-cited, but hitherto untested, case of morphological convergence is that between the aye-aye and squirrels. The aye-aye (Daubentonia madagascariensis) is a highly unusual lemuriform primate that has evolved a dentition similar to that of rodents: it possesses large, ever-growing incisors which it uses to strip the bark from trees in order to feed on wood-boring beetle larvae. Indeed, such is the similarity that some of the earliest classifications of the aye-aye placed it in the squirrel genus Sciurus Here, we aimed to test the degree of convergence between the skulls and lower jaws of squirrels and the aye-aye. Three-dimensional landmarks were recorded from the crania and mandibles of 46 taxa representing the majority of families in the Euarchontoglires. Results were plotted as phylomorphospaces and convergence measures were calculated. The convergence between squirrels and the aye-aye was shown to be statistically significant for both the cranium and mandible, although the mandibles seem to converge more closely in shape. The convergence may indicate strong functional drivers of morphology in these taxa, i.e. the use of the incisors to produce high bite forces during feeding. Overall, we have shown that this classic case of convergence stands up to quantitative analysis.

Do forelimb shape and peak forces co-vary in strepsirrhines?

OBJECTIVES: In this study, we explore whether ground reaction forces recorded during horizontal walking co-vary with the shape of the long bones of the forelimb in strepsirrhines. To do so, we quantify (1) the shape of the shaft and articular surfaces of each long bone of the forelimb, (2) the peak vertical, mediolateral, and horizontal ground reaction forces applied by the forelimb during arboreal locomotion, and (3) the relationship between the shape of the forelimb and peak forces. MATERIALS AND METHODS: Geometric morphometric approaches were used to quantify the shape of the bones. Kinetic data were collected during horizontal arboreal walking in eight species of strepsirrhines that show variation in habitual substrate use and morphology of the forelimb. These data were then used to explore the links between locomotor behavior, morphology, and mechanics using co-variation analyses in a phylogenetic framework. RESULTS: Our results show significant differences between slow quadrupedal climbers (lorises), vertical clinger and leapers (sifaka), and active arboreal quadrupeds (ring-tailed lemur, ruffed lemur) in both ground reaction forces and the shape of the long bones of the forelimb, with the propulsive and medially directed peak forces having the highest impact on the shape of the humerus. Co-variation between long bone shape and ground reaction forces was detected in both the humerus and ulna even when accounting for differences in body mass. DISCUSSION: These results demonstrate the importance of considering limb-loading beyond just peak vertical force, or substrate reaction force. A re-evaluation of osseous morphology and functional interpretations is necessary in light of these findings.

Do Muscles Constrain Skull Shape Evolution in Strepsirrhines?

Despite great interest and decades of research, the musculoskeletal relationships of the masticatory system in primates are still not fully understood. However, without a clear understanding of the interplay between muscles and bones it remains difficult to understand the functional significance of morphological traits of the skeleton. Here, we aim to study the impacts of the masticatory muscles on the shape of the cranium and the mandible as well as their co-variation in strepsirrhine primates. To do so, we use 3D geometric morphometric approaches to assess the shape of each bone of the skull of 20 species for which muscle data are available in the literature. Impacts of the masticatory muscles on the skull shape were assessed using non-phylogenetic regressions and phylogenetic regressions whereas co-variations were assessed using two-blocks partial least square (2B-PLS) and phylogenetic 2B-PLS. Our results show that there is a phylogenetic signal for skull shape and masticatory muscles. They also show that there is a significant impact of the masticatory muscles on cranial shape but not as much as on the mandible. The co-variations are also stronger between the masticatory muscles and cranial shape even when taking into account phylogeny. Interestingly, the results of co-variation between the masticatory muscles and mandibular shape show a more complex pattern in two different directions to get strong muscles associated with mandibular shape: a folivore way (with the bamboo lemurs and sifakas) and a hard-object eater one (with the aye-aye). Anat Rec, 301:291-310, 2018. © 2018 Wiley Periodicals, Inc.

Another look at the foramen magnum in bipedal mammals.

A more anteriorly positioned foramen magnum evolved in concert with bipedalism at least four times within Mammalia: once in macropodid marsupials, once in heteromyid rodents, once in dipodid rodents, and once in hominoid primates. Here, we expand upon previous research on the factors influencing mammalian foramen magnum position (FMP) and angle with four new analyses. First, we quantify FMP using a metric (basioccipital ratio) not previously examined in a broad comparative sample of mammals. Second, we evaluate the potential influence of relative brain size on both FMP and foramen magnum angle (FMA). Third, we assess FMP in an additional rodent clade (Anomaluroidea) containing bipedal springhares (Pedetes spp.) and gliding/quadrupedal anomalures (Anomalurus spp.). Fourth, we determine the relationship between measures of FMP and FMA in extant hominoids and an expanded mammalian sample. Our results indicate that bipedal/orthograde mammals have shorter basioccipitals than their quadrupedal/non-orthograde relatives. Brain size alone has no discernible effect on FMP or FMA. Brain size relative to palate size has a weak influence on FMP in some clades, but effects are not evident in all metrics of FMP and are inconsistent among clades. Among anomaluroids, bipedal Pedetes exhibits a more anterior FMP than gliding/quadrupedal Anomalurus. The relationship between FMA and FMP in hominoids depends on the metric chosen for quantifying FMP, and if modern humans are included in the sample. However, the relationship between FMA and FMP is nonexistent or weak across rodents, marsupials, and, to a lesser extent, strepsirrhine primates. These results provide further evidence that bipedal mammals tend to have more anteriorly positioned foramina magna than their quadrupedal close relatives. Our findings also suggest that the evolution of FMP and FMA in hominins may not be closely coupled.

Membranous Support for Eyes of Strepsirrhine Primates and Fruit Bats.

Living primates have relatively large eyes and support orbital tissues with a postorbital bar (POB) and/or septum. Some mammals with large eyes lack a POB, and presumably rely on soft tissues. Here, we examined the orbits of four species of strepsirrhine primates (Galagidae, Cheirogaleidae) and three species of fruit bats (Pteropodidae). Microdissection and light microscopy were employed to identify support structures of the orbit. In bats and primates, there are two layers of fascial sheets that border the eye laterally. The outer membrane is the most superficial layer of deep fascia, and has connections to the POB in primates. In fruit bats, which lacked a POB or analogous ligament, the deep fascia is reinforced by transverse ligaments. Bats and primates have a deeper membrane supporting the eye, identified as the periorbita (PA) based on the presence of elastic fibers and smooth muscle. The PA merges with periostea deep within the orbit, but has no periosteal attachment to the POB of primates. These findings demonstrate that relatively big eyes can be supported primarily with fibrous connective tissues as well as the PA, in absence of a POB or ligament. The well-developed smooth muscle component within the PA of fruit bats likely helps to protrude the eye, maintaining a more convergent eye orientation, with greater overlap of the visual fields. The possibility should be considered that early euprimates, and even stem primates that may have lacked a POB, also had more convergent eyes than indicated by osseous measurements of orbital orientation. Anat Rec, 299:1690-1703, 2016. © 2016 Wiley Periodicals, Inc.

Tempo does not correlate with mode in the fossil record.

The dominating view of evolution based on the fossil record is that established species remain more or less unaltered during their existence. Substantial evolution is on the other hand routinely reported for contemporary populations, and most quantitative traits show high potential for evolution. These contrasting observations on long- and short-time scales are often referred to as the paradox of stasis, which rests on the fundamental assumption that periods of morphological stasis in the fossil record represent minimal evolutionary change. Investigating 450 fossil time series, I demonstrate that the nonaccumulating morphological fluctuations during stasis travel similar distances in morphospace compared to lineages showing directional change. Hence, lineages showing stasis are commonly undergoing considerable amounts of evolution, but this evolution does not accumulate to produce large net evolutionary changes over time. Rates of evolutionary change across modes in the fossil record may be more homogenous than previously assumed and advocated, supporting the claim that substantial evolution is not exclusively or causally linked to the process of speciation. Instead of exemplifying minimal evolution, stasis likely represents information on the dynamics of the adaptive landscape on macroevolutionary time scales, including the persistence of adaptive zones and ecological niches over millions of years.

New euprimate postcrania from the early Eocene of Gujarat, India, and the strepsirrhine-haplorhine divergence.

The oldest primates of modern aspect (euprimates) appear abruptly on the Holarctic continents during a brief episode of global warming known as the Paleocene-Eocene Thermal Maximum, at the beginning of the Eocene (∼56 Ma). When they first appear in the fossil record, they are already divided into two distinct clades, Adapoidea (basal members of Strepsirrhini, which includes extant lemurs, lorises, and bushbabies) and Omomyidae (basal Haplorhini, which comprises living tarsiers, monkeys, and apes). Both groups have recently been discovered in the early Eocene Cambay Shale Formation of Vastan lignite mine, Gujarat, India, where they are known mainly from teeth and jaws. The Vastan fossils are dated at ∼54.5 Myr based on associated dinoflagellates and isotope stratigraphy. Here, we describe new, exquisitely preserved limb bones of these Indian primates that reveal more primitive postcranial characteristics than have been previously documented for either clade, and differences between them are so minor that in many cases we cannot be certain to which group they belong. Nevertheless, the small distinctions observed in some elements foreshadow postcranial traits that distinguish the groups by the middle Eocene, suggesting that the Vastan primates-though slightly younger than the oldest known euprimates-may represent the most primitive known remnants of the divergence between the two great primate clades.

Lower molar shape and size in prosimian and platyrrhine primates.

The goal of this research is to evaluate the relative strength of the influences of diet, size, and phylogenetic signal on dental geometric shape. Accurate comprehension of these factors and their interaction is important for reconstructing diet and deriving characters for a cladistic analysis in fossil primates. Geometric morphometric analysis is used to identify axes of shape variation in the lower second molars of (a) prosimian primates and (b) platyrrhines. Landmarks were placed on µCT-generated surface renderings. Landmark configurations were aligned using generalized Procrustes analysis. Principal components analysis and phylogenetic principal components analysis (pPCA) were performed on species average landmark co-ordinates. pPCs were examined with phylogenetic generalized least squares analysis for association with size and with diet. PCs from both phylogenetic and non-phylogenetic analyses were sufficient to separate species by broad dietary categories, including insectivores and folivores. In neither analysis was pPC1 correlated with tooth size, but some other pPCs were significantly correlated with size. The pattern of association between pPCs and size altered when centroid size and dietary variables were combined in the model; effects of diet factors typically exceeded effects of size. These results indicate a dominant phylogenetic and dietary signal in molar shape but also show some shape change correlated with size in the absence of obvious dietary associations. Geometric morphometric analysis appears to be useful for tracking functional traits in molars, particularly in tracking differences between folivorous and insectivorous species.

Locomotor pattern fails to predict foramen magnum angle in rodents, strepsirrhine primates, and marsupials.

Foramen magnum position has traditionally been used as an indicator of bipedality because it has been thought to favor a more "balanced" skull position. Here, we analyzed foramen magnum angle (FMA) in relation to locomotion in three mammalian orders that include bipedal or orthograde species in addition to quadrupedal or pronograde species. In marsupials and strepsirrhine primates, we found that there is no relationship between locomotor pattern and FMA. In rodents, we found that there is a significant difference in FMA between bipedal and quadrupedal rodents. However, when these species are analyzed in the context of enlarged auditory bullae, this relationship is no longer significant. Additionally, we find a significant relationship between relative brain size and FMA in strepsirrhine primates. Taken together, these data indicate that several developmental modules of the cranium influence FMA, but that locomotion does not. We caution that basicranial evolution is a complex phenomenon that must be explored in the context of each taxon's unique evolutionary and developmental history.

Reversible Deactivation of Motor Cortex Reveals Functional Connectivity with Posterior Parietal Cortex in the Prosimian Galago (Otolemur garnettii).

We examined the functional macrocircuitry of frontoparietal networks in the neocortex of prosimian primates (Otolemur garnettii) using a microfluidic thermal regulator to reversibly deactivate selected regions of motor cortex (M1). During deactivation of either forelimb or mouth/face movement domains within M1, we used long-train intracortical microstimulation techniques to evoke movements from the rostral division of posterior parietal cortex (PPCr). We found that deactivation of M1 movement domains in most instances abolished movements evoked in PPCr. The most common effect of deactivating M1 was to abolish evoked movements in a homotopic domain in PPCr. For example, deactivating M1 forelimb lift domains resulted in loss of evoked movement in forelimb domains in PPCr. However, at some sites, we also observed heterotopic effects; deactivating a specific domain in M1 (e.g., forelimb lift) resulted in loss of evoked movement in a different movement domain in PPCr (e.g., hand-to-mouth or eye-blink). At most sites examined in PPCr, rewarming M1 resulted in a reestablishment of the baseline movement at the same amplitude as that observed before cooling. However, at some sites, reactivation did not result in a return to baseline movement or to the full amplitude of the baseline movement. We discuss our findings in the context of frontoparietal circuits and how they may subserve a repertoire of ecologically relevant behaviors. SIGNIFICANCE STATEMENT: The posterior parietal cortex (PPC) of primates integrates sensory information used to guide movements. Different modules within PPC and motor cortex (M1) appear to control various motor behaviors (e.g., reaching, defense, and feeding). How these modules work together may vary across species and may explain differences in dexterity and even the capacity for tool use. We investigated the functional connectivity of these modules in galagos, a prosimian primate with relatively simple frontoparietal circuitry. By deactivating a reaching module in M1, we interfered with the function of similar PPC modules and occasionally unrelated PPC modules as well (e.g., eye blink). This circuitry in galagos, therefore, is more complex than in nonprimates, indicating that it has been altered with the expansion of primate PPC.