Jonathan M. G. Perry

Convergent evolution of anthropoid-like adaptations in Eocene adapiform primates

Adapiform or ‘adapoid’ primates first appear in the fossil record in the earliest Eocene epoch (∼55 million years (Myr) ago), and were common components of Palaeogene primate communities in Europe, Asia and North America. Adapiforms are commonly referred to as the ‘lemur-like’ primates of the Eocene epoch, and recent phylogenetic analyses have placed adapiforms as stem members of Strepsirrhini, a primate suborder whose crown clade includes lemurs, lorises and galagos. An alternative view is that adapiforms are stem anthropoids. This debate has recently been rekindled by the description of a largely complete skeleton of the adapiform Darwinius, from the middle Eocene of Europe, which has been widely publicised as an important ‘link’ in the early evolution of Anthropoidea. Here we describe the complete dentition and jaw of a large-bodied adapiform (Afradapis gen. nov.) from the earliest late Eocene of Egypt (∼37 Myr ago) that exhibits a striking series of derived dental and gnathic features that also occur in younger anthropoid primates—notably the earliest catarrhine ancestors of Old World monkeys and apes. Phylogenetic analysis of 360 morphological features scored across 117 living and extinct primates (including all candidate stem anthropoids) does not place adapiforms as haplorhines (that is, members of a Tarsius–Anthropoidea clade) or as stem anthropoids, but rather as sister taxa of crown Strepsirrhini; Afradapis and Darwinius are placed in a geographically widespread clade of caenopithecine adapiforms that left no known descendants. The specialized morphological features that these adapiforms share with anthropoids are therefore most parsimoniously interpreted as evolutionary convergences. As the largest non-anthropoid primate ever documented in Afro-Arabia, Afradapis nevertheless provides surprising new evidence for prosimian diversity in the Eocene of Africa, and raises the possibility that ecological competition between adapiforms and higher primates might have played an important role during the early evolution of stem and crown Anthropoidea in Afro-Arabia.

The Jaw Adductors of Strepsirrhines in Relation to Body Size, Diet, and Ingested Food Size

Body size and food properties account for much of the variation in the hard tissue morphology of the masticatory system whereas their influence on the soft tissue anatomy remains relatively understudied. Data on jaw adductor fiber architecture and experimentally determined ingested food size in a broad sample of 24 species of extant strepsirrhines allows us to evaluate several hypotheses about the influence of body size and diet on the masticatory muscles. Jaw adductor mass scales isometrically with body mass (β = 0.99, r = 0.95), skull size (β = 1.04, r = 0.97), and jaw length cubed (β = 1.02, r = 0.95). Fiber length also scales isometrically with body mass (β = 0.28, r = 0.85), skull size (β = 0.33, r = 0.84), and jaw length cubed (β = 0.29, r = 0.88). Physiological cross‐sectional area (PCSA) scales with isometry or slight positive allometry with body mass (β = 0.76, r = 0.92), skull size (β = 0.78, r = 0.94), and jaw length cubed (β = 0.78, r = 0.91). Whereas PCSA is isometric to body size estimates in frugivores, it is positively allometric in folivores. Independent of body size, fiber length is correlated with maximum ingested food size, suggesting that ingestive gape is related to fiber excursion. Comparisons of temporalis, masseter, and medial pterygoid PCSA in strepsirrhines of different diets suggest that there may be functional partitioning between these muscle groups. Anat Rec, 2011.

Bite Force Estimation and the Fiber Architecture of Felid Masticatory Muscles

Increasingly, analyses of craniodental dietary adaptations take into account mechanical properties of foods. However, masticatory muscle fiber architecture has been described for relatively few lineages, even though an understanding of the scaling of this anatomy can yield important information about adaptations for stretch and strength in the masticatory system. Data on the mandibular adductors of 28 specimens from nine species of felids representing nearly the entire body size range of the family allow us to evaluate the influence of body size and diet on the masticatory apparatus within this lineage. Masticatory muscle masses scale isometrically, tending toward positive allometry, with body mass and jaw length. This allometry becomes significant when the independent variable is a geometric mean of cranial variables. For all three body size proxies, the physiological cross‐sectional area and predicted bite forces scale with significant positive allometry. Average fiber lengths (FL) tend toward negative allometry though with wide confidence intervals resulting from substantial scatter. We believe that these FL residuals are affected by dietary signals within the sample; though the mechanical properties of felid diets are relatively similar across species, the most durophagous species in our sample (the jaguar) appears to have relatively higher force production capabilities. The more notable dietary trend in our sample is the relationship between FL and relative prey size: felid species that predominantly consume relatively small prey have short masticatory muscle fibers, and species that regularly consume relatively large prey have relatively long fibers. This suggests an adaptive signal related to gape. Anat Rec, 2012.

A fossil primate of uncertain affinities from the earliest late Eocene of Egypt

Paleontological work carried out over the last 3 decades has established that three major primate groups were present in the Eocene of Africa—anthropoids, adapiforms, and advanced strepsirrhines. Here we describe isolated teeth of a previously undocumented primate from the earliest late Eocene (≈37 Ma) of northern Egypt, Nosmips aenigmaticus, whose phylogenetic placement within Primates is unclear. Nosmips is smaller than the sympatric adapiform Afradapis but is considerably larger than other primate taxa known from the same paleocommunity. The species bears an odd mosaic of dental features, combining enlarged, elongate, and molariform premolars with simple upper molars that lack hypocones. Phylogenetic analysis across a series of different assumption sets variously places Nosmips as a stem anthropoid, a nonadapiform stem strepsirrhine, or even among adapiforms. This phylogenetic instability suggests to us that Nosmips likely represents a highly specialized member of a previously undocumented, and presumably quite ancient, endemic African primate lineage, the subordinal affinities of which have been obscured by its striking dental autapomorphies. Discriminant functions based on measurements of lower molar size and topography reliably classify extant prosimian primates into their correct dietary groups and identify Nosmips and Afradapis as omnivores and folivores, respectively. Although Nosmips currently defies classification, this strange and unexpected fossil primate nevertheless provides additional evidence for high primate diversity in northern Africa ≈37 million years ago and further underscores the fact that our understanding of early primate evolution on that continent remains highly incomplete.

Maximum ingested food size in captive strepsirrhine primates: Scaling and the effects of diet

Little is known about ingested food size (V(b)) in primates, even though this variable has potentially important effects on food intake and processing. This study provides the first data on V(b) in strepsirrhine primates using a captive sample of 17 species. These data can be used for generating and testing models of feeding energetics. Strepsirrhines are of interest because they are hypometabolic and chewing rate and daily feeding time do not show a significant scaling relationship with body size. Using melon, carrot, and sweet potato we found that maximum V(b) scales isometrically with body mass and mandible length. Low dietary quality in larger strepsirrhines might explain why V(b) increases with body size at a greater rate than does resting metabolic rate. Relative to body size, V(b) is large in frugivores but small in folivores; furthermore scaling slopes are higher in frugivores than in folivores. A gross estimate of dietary quality explains much of the variation in V(b) that is not explained by body size. Gape adaptations might favor habitually large bites for frugivores and small ones for folivores. More data are required for several feeding variables and for wild populations.

PHYLOGENETIC, ECOLOGICAL, AND ALLOMETRIC CORRELATES OF CRANIAL SHAPE IN MALAGASY LEMURIFORMS

Adaptive radiations provide important insights into many aspects of evolution, including the relationship between ecology and morphological diversification as well as between ecology and speciation. Many such radiations include divergence along a dietary axis, although other ecological variables may also drive diversification, including differences in diel activity patterns. This study examines the role of two key ecological variables, diet and activity patterns, in shaping the radiation of a diverse clade of primates, the Malagasy lemurs. When phylogeny was ignored, activity pattern and several dietary variables predicted a significant proportion of cranial shape variation. However, when phylogeny was taken into account, only typical diet accounted for a significant proportion of shape variation. One possible explanation for this discrepancy is that this radiation was characterized by a relatively small number of dietary shifts (and possibly changes in body size) that occurred in conjunction with the divergence of major clades. This pattern may be difficult to detect with the phylogenetic comparative methods used here, but may characterize not just lemurs but other mammals.

The Jaw Adductor Resultant and Estimated Bite Force in Primates

We reconstructed the jaw adductor resultant in 34 primate species using new data on muscle physiological cross-sectional area (PCSA) and data on skull landmarks. Based on predictions by Greaves, the resultant should (1) cross the jaw at 30% of its length, (2) lie directly posterior to the last molar, and (3) incline more anteriorly in primates that need not resist large anteriorly-directed forces. We found that the resultant lies significantly posterior to its predicted location, is significantly posterior to the last molar, and is significantly more anteriorly inclined in folivores than in frugivores. Perhaps primates emphasize avoiding temporomandibular joint distraction and/or wide gapes at the expense of bite force. Our exploration of trends in the data revealed that estimated bite force varies with body mass (but not diet) and is significantly greater in strepsirrhines than in anthropoids. This might be related to greater contribution from the balancing-side jaw adductors in anthropoids.

Comparing apples and oranges—the influence of food mechanical properties on ingestive bite sizes in lemurs

Previously we found that Maximum Ingested Bite Size (Vb )-the largest piece of food that an animal will ingest whole without biting first-scales isometrically with body size in 17 species of strepsirrhines at the Duke Lemur Center (DLC). However, because this earlier study focused on only three food types (two with similar mechanical properties), it did not yield results that were easily applied to describing the broad diets of these taxa. Expressing Vb in terms of food mechanical properties allows us to compare data across food types, including foods of wild lemurs, to better understand dietary adaptations in lemurs. To this end, we quantified Vb in five species of lemurs at the DLC representing large and small frugivores and folivores using ten types of food that vary widely in stiffness and toughness to determine how these properties relate to bite sizes. We found that although most species take smaller bites of stiffer foods, this negative relationship was not statistically significant across the whole sample. However, there is a significant relationship between bite size and toughness. All three of the more frugivorous taxa in our sample take significantly smaller bites of tougher foods. However, the two more folivorous lemurs do not. They take small bites for all foods. This suggests that the species most adapted to the consumption of tough foods do not modulate their ingestive sizes to accommodate larger pieces of weak foods.

Tooth Root Size, Chewing Muscle Leverage, and the Biology of Homunculus patagonicus (Primates) from the late early Miocene of Patagonia

Abstract. Inferences about the diet of Miocene platyrrhine monkeys have relied upon the morphology of the molar teeth, specifically the crests on the molars. Using a library of Micro-CT images of a broad comparative sample of living platyrrhines (callitrichines, cebines, pitheciids and atelids), late early Miocene Homunculus, and the early Miocene Tremacebus and Dolichocebus, we extend these inferences by examining the surface areas of the tooth roots, anchor points for the periodontal ligaments. From muscle scars on the skull, we estimate the mechanical leverage of the chewing muscles at bite points from the canine to the last molar. Extant platyrrhines that gouge bark to obtain exudates do not have especially large canine roots or anterior premolar roots compared with their less specialized close relatives. Extant platyrrhines that have more folivorous diets have much larger molar roots than do similar-sized more frugivorous species. Homunculus patagonicus has large postcanine roots relative to body size and poor masticatory leverage compared to the extant platyrrhines in our sample. The large postcanine roots, heavy tooth wear, and moderately-long shearing crests suggests a diet of abrasive, resistant foods. However, relatively poor jaw adductor leverage would have put the masticatory apparatus of Homunculus at a mechanical disadvantage for producing high bite forces compared to the condition in extant platyrrhines. Tremacebus and Dolichocebus, like Homunculus, have larger tooth root surfaces than comparable-sized living platyrrhines. They also resemble Homunculus in being more prognathic and having posteriorly-located temporalis origins - all features of a relatively poor leverage system.

Maximum ingested food size in captive anthropoids.

OBJECTIVES Maximum ingested food size (Vb ) is an empirically tested performance variable that can shed light on feeding energetics and adaptation in the masticatory system. Until now, this variable had been tested in strepsirrhines alone among primates. Here, we present the first data on Vb in a broad sample of anthropoid primates and describe scaling patterns. MATERIALS AND METHODS Vb data on anthropoids were collected under captive conditions at the Philadelphia Zoo and compared with published data on strepsirrhines. Data on Vb were scaled against individual body mass and were compared with experimentally determined toughness and stiffness values for the test foods. RESULTS Unlike in strepsirrhines, where essentially Vb scales isometrically with body mass, Vb in anthropoids scales with negative allometry. There is a significant effect of food material properties on Vb , although bite size in anthropoids varies less based on food properties than in strepsirrhines. Large folivorous strepsirrhines follow the anthropoid trend in bite size scaling, but large frugivorous ones take especially large bites. DISCUSSION Negative scaling of bite size in the anthropoids sampled could be due to reduced adaptation for gape. Some early anthropoids likely evolved adaptations for maximizing mechanical advantage and fatigue resistance in the chewing muscles, resulting in reduced gape. This might have channeled them toward smaller bites of more-resistant foods and away from taking large bites. This might also be the case for some folivorous strepsirrhines.