Fallback Foods, Preferred Foods, Adaptive Zones, and Primate Origins

American Journal of Primatology 9999:1–8 (2013)

COMMENTARY Fallback Foods, Preferred Foods, Adaptive Zones, and Primate Origins

ALFRED L. ROSENBERGER1,2,3,4* 1Department of Anthropology and Archaeology, Brooklyn College, CUNY, Brooklyn, New York 2Department of Anthropology, City University of New York Graduate Center, New York, New York 3Consortium in Evolutionary Primatology (NYCEP), New York, New York 4Department of Mammals, American Museum of Natural History, New York, New York Appreciation has grown for the impact of tropical forest seasonality and fallback foods on primate diets, behaviors, and morphology. As critically important resources in times of shortage, seasonal fallback foods may have an outsized role in selecting for form and function while the diversity of preferred plant foods has played an equally prominent role in shaping primate evolution. Here, hypotheses of primate origins are examined in the context of food choice models developed by Marshall and Wrangham [2007] and related to the broader concepts of adaptive zones and radiations. The integrated evolution of primate diet and positional behavior is consistent with a growing reliance on angiosperm products—not prey—as preferred and seasonal fallback foods, temporally and phylogenetically coordinated with evolutionary phases of the angiosperm adaptive radiation. Selection for an incisor oriented but non‐specialized heterodont dentition, in contrast with most other orders, attests to the universal role of a highly varied vegetation diet as the primates’ primary food resource, with diverse physical properties, phenology and high seasonality. A preference by plesiadapiforms for eating small protein‐ and lipid‐rich seeds may have predisposed the primates and advanced angiosperms to diversify their evolving ecological interdepen- dence, which established the primate adaptive zone and became realized more fully with the rise of the modern euprimate and angiosperm phenotypes. The “narrow niche” hypothesis, a recent challenge to the angiosperm co‐evolution hypothesis, is evaluated further. Finally, I note support for visual predation as a core adaptive breakthrough for primates or euprimates remains elusive and problematic, especially considering the theoretical framework provided by the Marshall–Wrangham model, updated evidence of primate feeding habits and the counterpoint lessons of the most successful primate predators, the tarsiiforms. Am. J. Primatol. 9999:1–8, 2013. © 2013 Wiley Periodicals, Inc.

Key words: seasonal fallback foods; primate origins; adaptive zones; angiosperms; visual predation

INTRODUCTION principles with which to test, elaborate and/or refocus Recent compendia [Constantino and Wright, 2009; competing adaptive hypotheses. Here, I concentrate Cuozzo et al., 2012] have added to our understanding of primarily on the implications for the fruit eating primate diets and dentition, with important implica- hypothesis [Szalay, 1968] and the visual predation tions for defining the primate adaptive zone and hypothesis [Cartmill, 1974]. The primate/angiosperm ‐ reconstructing primate origins. Like other orders of co evolution hypothesis [Sussman, 1991], recently mammals [Osborn, 1902; Simpson, 1953; Van reviewed in this journal [Sussman et al., 2012], is not ‐ fi Valen, 1971], the primate adaptive radiation occupies treated separately since co evolution was by de nition an exclusive ecological domain made possible by a prevalent, driving factor in primate evolution, distinctive key characteristics—Osborn stressed morphological combinations underlying locomotion and diet—that evolved in response to environmental Conflicts of interest: None. Ã parameters, location of food, and mode of food acquisi- Correspondence to: Alfred L. Rosenberger, Department of Anthropology and Archaeology, Brooklyn College, CUNY, tion. While participants in the ongoing debate on Brooklyn, New York. E‐mail: [email protected] primate origins [e.g., Bloch et al., 2007; Cartmill, 1992; Received 11 January 2013; revised 8 April 2013; revision Sargis et al., 2007; Silcox et al., 2007a,b; Soligo and accepted 8 April 2013 Martin, 2006] are keenly intent to explain anatomical DOI: 10.1002/ajp.22162 features in the context of the arboreal milieu in which Published online XX Month Year in Wiley Online Library primates first evolved, new studies present a fresh set of (wileyonlinelibrary.com).

although a critique by Orkin and Pontzer [2011] tion than earlier efforts based on linear features warrants attention. Nor is it necessary to distinguish [e.g., Kay, 1975 et seq.], tend to illustrate a derivatives such as the grasp‐leaping hypothesis stronger linkage between adaptive morphology [Szalay and Dagosto, 1980] or the nocturnal visual and SFBFs than with more conventional dietary predation hypothesis [Ravosa et al., 2000], which have classifications (frugivore, insectivore, folivore) of more to do with euprimates than with primates sensu species [Boyer, 2008]. Having said that, it is lato. Accordingly, to avoid confusion over terms and nevertheless important to recognize examples taxonomic concepts, particularly how authors variously where species and even higher taxonomic groups, compose the Order Primates, the taxonomy employed such as platyrrhine pitheciins, have adapted by here is made clear: plesiadapiforms are stem primates making challenging foods their standard, non‐ [e.g., Bloch et al., 2007]; euprimates consist of seasonal PFs. In fact, successfully shifting feeding strepsirhines, including fossil adapiforms, and haplor- adaptations employed at times of scarcity toward hines, including anthropoids and tarsiiforms. seasonally abundant foods has been suggested as a key to the origins of this group [Rosenberger, 1992]. Food, feeding and adaptation Food scarcity is a fact of primate life, as even It is now evident from in‐depth, long‐term field tropical forests are cyclically influenced by climate studies across all radiations that primate feeding and weather [van Schaik and Pfannes, 2005], bring- strategies are strongly influenced by shortages. ing the evolutionary roles of PFs and SFBFs Rarely eaten foods appear to often be a more salient sharply into focus. The pressure of food shortages and widespread source of selection for feeding exists in spite of the great biodiversity of the tropics adaptations than commonly eaten foods or overall and the enormous numbers of plant species primates consumption [see Constantino and Wright, 2009; consume. Faced with seasonally depleted PFs, Cuozzo et al., 2012; van Schaik and Pfannes, 2005]. primates do not migrate, hibernate, or cache food to The selective role of uncommon foods was intro- tide them over like many other mammals. They duced in morphology as the critical‐function hy- switch to SFBFs. New leaves, mature leaves and pothesis [Rosenberger, 1992; Rosenberger and vegetable matter rank highest as SFBFs, followed by Kinzey, 1976]: in the interaction between organism fruits and animals [Hemingway and Bynum, 2005], and environment, behaviors that involve more but the rarity and taxonomic distribution of primates challenging biomechanical requirements govern feeding on animals as SFBFs indicates this coping the evolution of form. Field workers developed an strategy is not an easily utilized option. Two of the ecological compliment to the critical‐function hy- five taxa that regularly do are persistently preda- pothesis, the fallback foods hypothesis [e.g., ceous, specialized clades, cebines and callitrichines, Lambert, 2007; Lambert et al., 2004], and Marshall while there are no morphological suggestions that and Wrangham [2007] extended this synthetic animalivory has imposed significant selective pres- model by redefining primate dietary categories sure on the others, the several pitheciins, lemurids operationally, thus providing a framework for and cercopithecines. Obligate animalivory, either integrating adaptive characteristics across ana- as a PF or SFBF, should thus be regarded as a tomical systems. While these associations are often highly specialized primate diet, present in tarsiers, acknowledged, they are rarely correlated robustly some platyrrhines, and lorisiforms [see Campbell or have their connectivity grounded in theory. In et al., 2011] that exhibit complexes of unique the Marshall–Wrangham paradigm, preferred predatory adaptations. foods (PFs) are chosen more often than would be expected given their temporal‐spatial abundance in a habitat, and they provide a plentiful source of The Primate Adaptive Zone easily consumed calories. Thus, collecting PFs Discussion of adaptive zones and reconstructed drives selection of sensory, cognitive and position- origins must assume continuity between modern and al/locomotor adaptations. Fallback foods are non‐ past conditions and focus on synergistic attributes of preferred but highly important seasonally,when ecology and morphology. The concept of an ordinal PFs are scarce. To emphasize their seasonal adaptive zone is also restrictively multiplicative: once nature, and the point that this is not a rare the niche is attained in the group’s ancestry by virtue phenomenon but a regular and consistent part of of key adaptations, essentially all descendant mem- evolutionary adaptation, I refer to them as seasonal bers of that radiation are expected to exhibit the fallback foods (SFBFs). SFBFs are typically abun- lifestyle made possible by those traits, with few dant but may be hard to process, requiring special- exceptions but potentially many variations. Thus, izations to access, ingest, masticate or digest. basically all carnivorans slice flesh to eat, some in Recent empirical studies that attempt to take aquatic environments but most on land; all rodents into account the three‐dimensional structure of tooth‐gouge to feed, some as arboreal gliders but most molars, thus capturing more functional informa- as ground dwellers; all artiodactyls grind leaves or

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grass, some amphibiously but most in relatively open versatile cheek teeth reflect the broad range of country. physical properties a primate encounters consuming For primates, several parameters and synergistic a wide variety of vegetation. They evidence a basal, attributes frame the analysis. (1) Primates are an frugivorous PF diet with the potential for evolving arboreal tropical radiation and experience seasonal morphological compromises extending the dentition food scarcity. (2) Fruits constitute the basic PF diet to permit efficient consumption of arthropods or and vegetation remains favored as SFBFs during leaves as well, which only require modest shape periods of scarcity. (3) Primate dentitions are changes to augment puncturing, cutting or shearing characteristically eutherian‐primitive, retaining a potential [e.g., Kay and Hiiemae, 1974; Rosenberger heterodont pattern without dramatic modifications and Kinzey, 1976]. Rather than emphasizing the for harvesting or processing a narrow food class. (4) comparatively primitive and retentive nature of the Primates are athletic, generalized locomotors with primate dentition in a non‐ecological context [e.g., prehensile cheiridia and deploy an enormous behav- Clark, 1959], it is more instructive to regard its ioral repertoire to meet ever‐changing substrate inherent biomechanical flexibility as an asset under conditions. (5) Primate vision emphasizes a central- selection, balancing the varied physical properties of ized binocular gaze and good close‐range depth primate foods. perception as opposed to a large field of view and As the digestive system’s point of contact monocular peripheral vision. between the organism and the environment, incisors One can now reformulate Van Valen’s [1971] (like cheiridia) are exquisitely sensitive to selection. primate adaptive zone: a tropical, arboreal, seasonally This makes it noteworthy that non‐tarsiiform eupri- challenging domain where a wide variety of fruits are mate dentitions commonly present cropping incisors PFs and a narrower spectrum of fruits, plus leaves and for harvesting fruit and foliage. While especially other vegetation are principal SFBFs. This constrains evident among the spatulate‐incisored anthropoids, predictions regarding ancestral primate anatomy and lemuriform strepsirhines also have wide upper guards against reductionism or over‐generalization. incisors, though comparatively reduced in height While a single molar tooth may be a proper object of and thickness, a configuration more than serviceable considerationininvestigatingprimateorigins,it for harvesting vegetation, for example, stripping typically can only address part of a primate’sdietary leaves without employing a hard bite against the profile [Rosenberger, 2010a]. Other factors may be often delicate toothcomb. In conjunction with the required to elucidate SFBFs, or to identify the most relatively low metabolism of extant species [Snod- challenging items fed upon or encountered in accessing grass et al., 2007], this suggests leaves were impor- foods, and knowledge of many facets is required to tant to basal strepsirhines. Among them, the establish overall niche. For instance, while both Aloutta primitive notharctid adapiforms have upper incisors and Brachyteles each have well documented “folivo- closely resembling those of lemuriforms [e.g., Rose- rous” molars, they differ profoundly in cranial, skeletal nberger et al., 1985], spatulate lower incisors and and gut anatomy, relative brain size, sociality, and use bunodont, moderately crested molar teeth of space. Beyond dental adaptations, only Alouatta [Gilbert, 2005], a combination suitable for fruits as conforms bodily and behaviorally to the folivory model PFs and other vegetation as SFBFs. The dentally [Rosenberger et al., 2011]. derived adapids have more advanced cropping incisors, more crested cheek teeth and, in cases where it is well documented, a less agile postcranium DISCUSSION [Dagosto, 1983; Gebo, 1988], possibly suggesting a shift to a predominantly semi‐folivorous PF/SFBF Fruit As the Original Primate Diet diet analogous to the above mentioned large platyr- The Marshall–Wrangham [2007] model predicts rhines [Rosenberger et al., 2011]. that ancestral euprimates should have a generalized One outstanding nonhuman exception to these feeding system able to effectively harvest and generalizations about diet, dentition and adaptive zone masticate fruits with a wide variety of physical —a lesson in and of itself—involves tarsiers, which eat properties as PFs, a locomotor system to facilitate absolutely no plant material [Gursky, 2007]. In a way discovery of these fruits, a sensory system able to tarsiers present a functionally homodont dentition: to detect PFs reliably, and coordinated subsystems to the greatest possible extent, incisors, canine, premolars facilitate access, ingestion, mastication and digestion and molar cusps are configured as a series of piercing of seasonally useful fruit, leaves and other vegetation cones and cutting blades, with acutely cusped and as SFBFs. These predictions are borne out by the crested molar crowns presenting enhanced puncturing modern primate dentition. While diversified, it and shearing functions. They also have radically normally lacks constraining specializations – no specialized visual, cranial and postcranial adaptations razor sharp or milling teeth; no cheek tooth gaps designed to support the tarsier’smethodofpreycapture filled by storage pouches; only rare occurrences of [e.g., Rosenberger, 2011]. In contrast, despite their spiky premolar and molar crowns. Functionally equally small body size, the molars of most Eocene

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tarsiiform genera, and especially the basal anaptomor- with enlarged orbits, elongate feet and, as docu- phines, do not exhibit high levels of shearing mented at least in the former, a fused tibio‐fibula. [Strait, 2001] while their crania and postcrania present Plesiadapiforms were preadaptively disposed to galago‐like advances toward a tarsier‐like pattern in the ancestral euprimate vegetation diet but they did terms of orbital enlargement and leaping adaptations not pass a particular adaptive threshold. While the [e.g., Rosenberger and Preuschoft, 2012]. This indicates majority of the dental inferences discussed apply to a continued reliance on fruit coupled with a new them as well, various elements of the feeding‐locomotor capacity to exploit prey in a nocturnal milieu by system remain more primitive. Their bunodont, non- evolving novel—not primitive—features in combina- descript cheek teeth suggest a reliance on vegetation. tion. The marked departure from a “standard” eupri- Butatasmallbodysize[mostly<50–300 g: mate morphology across these systems, which as a Fleagle, 1999; see also Silcox et al., 2007a,b], meaning package is clearly antecedent to the Tarsius pattern, is also a proportionately short jaw length and limited an indication of the group’s shift to incorporate prey as gape, plesiadapiforms would have been restricted to a part of their PF menu, and the intense selective range of small, berry‐sized fruits, probably with a challenges associated with such a change. Thus any narrower spectrum of physical properties than modern super predatory members that may potentially be primates encounter. This is consistent with the found as fossils belonging to the exclusive tarsier characteristics of primitive angiosperms, which had lineage are likely to be adaptive outliers as well, with not yet evolved the modern features highly attractive to limited relevance to reconstructing the ancestral mammalian and avian seed dispersers. The conical tarsiiform or euprimate feeding and foraging central incisors of plesiadapiforms that distinguish strategies. them from modern euprimates probably relate to The first appearances of euprimates in the harvesting the early proto‐fruits. While frequently early Eocene [Gingerich, 1986; Ni et al., 2004; high‐crowned, proclivus and pointed in advanced Smith et al., 2006] co‐occur with a burst of Tertiary lineages, the simpler, primitive forms are aptly angiosperm biodiversity and innovation [e.g., Suss- designed for axial loading, used as a probe and/or man et al., 2012], including an increase in seed size pincer suitable for prying loose small pre‐Eocene fruits and predominance of closed‐canopy forests [e.g., and seeds [<10 mm: Tiffney, 2004] in beak‐like fashion Eriksson,2008;Tiffney,2004],thusforgingthe [Rosenberger, 2010b]. critical link between diet and locomotion anticipat- Seeds, in addition to fruit pulp and aril, play an ed by Osborn [1902]. Consistent with this ecological enormous role in the food webs of vertebrates and reconstruction is evidence that euprimates present invertebrates [Sallabanks and Courtney, 1992]. Al- a transformed locomotor system capable of power- though specialized seed harvesting has been inferred ful hindlimb grasping and leaping [e.g., for some highly modified plesiadapiforms as well, Dagosto, 1988]. Thus, at a moderate body size, such as the plagiaulacoid‐toothed carpolestids adapiformswouldhavebeenabletoforagewidely [Biknevicius, 1986], it is likely that wind dispersed through a continuous canopy via intersecting seeds played a broadly important role in plesiadapi- terminal branches, to locate an increasingly large form feeding [Rosenberger et al., 2011], perhaps more number of larger fruit species serving as PFs, using so than we have thought, for large‐seed, fleshy fruits enhanced sensory and cognitive means to detect were not as common during the late Cretaceous and them—relatively larger eyes and brains than the early parts of the Paleocene. Seed‐eating may have more primitive plesiadapiforms [Silcox et al., 2009]. predisposed stem primates to the ecological interde- Smaller forms would have also exploited angio- pendence attained during the Eocene among eupri- sperms in the understory where early phase mates and modern angiosperms. By then, larger, flowering plants were successful [Field fleshy fruit had evolved to attract pulp‐eating et al., 2004]. As noted, neither the majority of frugivorous animals [see Sussman et al., 2012] with adapiforms, nor all the tarsiiforms, evidence a desirable, energy‐rich alternative or compliment to widespread, advanced morphological indications seeds [Rosenberger et al., 2011], thus selectively of insectivory, although it is not possible to exclude promoting primates to evolve a new role as seed‐ asizeablesoft‐bodied insect fraction on the basis of disperser instead of seed‐predator. This transition is molar form. This is particularly true of the also marked by a shift in locomotor competence, for taxonomically diverse tarsiiforms. They radiated the non‐acrobatic arborealism of known plesiadapi- within a small body mass class and, as good leapers, forms [Bloch and Boyer, 2007; Sargis et al., 2007] probably were ecologically segregated by specializ- suggests wide‐ranging foraging to dispersed fruit ing in the use of the understory stratum. They also patches was not central to their PF pattern. Small present some unexpected cross‐system morpholog- eyes and lack of expansive, sensitive fingertips ical combinations. For example, as noted by Rose- indicate a less advanced form of food detection and nberger and Preuschoft [2012], the European manipulation, foraging travel and arboreal maneu- sister‐taxa Necrolemur and Microchoerus combine verability, in which pedal prehension may have been complex, low‐relief, non‐shearing molar crowns more advantageous for stable feeding postures and

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quadrupedal walking than gap‐crossing, acrobatic orders is never warranted. It is evident that locomotion [e.g., Bloch and Boyer, 2002]. arboreality comes in many forms, stemming from Since this line of reasoning coincides with the many alternative basal conditions involving different angiosperm co‐evolution hypothesis [Sussman, 1991], phyletic origins, evolutionary histories and con- it seems fitting to comment on a recent challenge, the straints, and it evolves with a variety of ecological “narrow niche” hypothesis of Orkin and Pontzer compromises regarding the degree and manner by [2011]. They pose the same question as Cartmill which taxa are adapted to the physicality of arboreal [1974] in his critique of the classic arboreal hypothesis life. At a basic level, squirrels are a flawed conver- of primate evolution: If foraging in terminal branches gence model and should not be expected to evolve introduced selective pressures that drove the evolu- many euprimate resemblances because they are tion of euprimate features, why are squirrels not more bound to an arbo‐terrestrial existence, foraging and like them? This appeal to an extrinsic extra‐ordinal sheltering in the trees but caching food on the ground, analogy as the primary explanatory model is a which selects for scansorialism. Their eyes, orbits and common method in origination studies—the presence skulls cannot be primate‐like because their heads of forward facing eyes in primates and cats means house a massively specialized, somewhat peculiar that primates are visual predators—and quite differ- masticatory apparatus that constrains its architec- ent from the perspective I share with Sussman et al. ture. (4) The Orkin‐Pontzer model also suffers [2012], which seeks to integrate functional morpholo- limitations in that it tries to explain only one gy with ecological rules generalized intrinsically from dimension of the primate adaptive zone. At a studies spanning the primate order and the notion of minimum, a truly robust origination model needs to mammalian adaptive zones [Van Valen, 1971]. account for and integrate adaptation to habitat, food, Orkin and Pontzer [2011] conclude from their use of space, and time of activity (which I admittedly study of squirrel arboreal locomotion that an addi- do not address here either). It requires a framework tional term must be included in the angiosperm that conforms to ecological principles derived from hypothesis to make end branches the springboard knowledge of primate patterns and universals, as in that selectively induced the primates’ derived loco- the Marshall–Wrangham paradigm [2007]. motor characteristics. They argue it is not the attainment of arboreal behaviors but the loss of others that effectively “narrowed” the euprimate Prey As The Original Primate Diet? niche from its broader, pre‐euprimate dimensions. I Emmons [2000], Muchlinski [2012], and Suss- see several difficulties with their argument: (1) It man et al. [2012] point out that among small non‐ turns on a difference in semantics and emphasis. By chiropteran mammals the predation niche is very insisting there is more heuristic value in specifying a rare and scattered taxonomically, save mostly for the “loss” of locomotor competence as opposed to the few specialized primates mentioned above. This widely acknowledged generalized “shift” in primate raises questions about its relevance to primate and positional behaviors, Orkin and Pontzer dwell on the euprimate [and anthropoid; see Ross, 2000] origins historical process by which euprimate attributes and its viability as an adaptive zone concept. The arose, whereas Sussman et al. [2012] seek to explain hypothesis that insect, arthropod or vertebrate prey the ecological context of a new realized niche. (2) By was the formative dietary component of euprimates failing to consider the entirety of fossil evidence in or plesiadapiforms is also difficult to reconcile with this evolutionary sequence, Orkin and Pontzer miss the Marshall–Wrangham [2007] model. Among the ecological attributes that their “loss” model extant primates, animals very rarely serve as PFs stipulates. Plesiadapiforms, in their scansorial ar- or SFBFs, so the universality criterion, or even a borealism, are arguably analogous to squirrels in lesser commonality standard, is not met: predation locomotor competence, so a reduction in claw‐based does not comply with the very notion of a primate locomotion without pedal grasping [Sargis adaptive zone shaping primate biodiversity. If et al., 2007] is inherently part of the transition predation was the ecological breakthrough that from that morphological gestalt toward the eupri- ushered in the primate ordinal niche, one would mate condition. This is precisely what many believe expect the majority of living primates to be obligate— happened as primates became adept at living among not variously facultative—predators, with animal- angiosperm terminals, including Szalay [1968], Cart- ivorous adaptations evident across bodily systems. mill [1974], and Sussman and Raven [1978]. (3) Orkin Neither fieldwork, dental or postcranial morphology and Pontzer apparently maintain that all small supports this. For example, while persistent stalking mammals living in the terminals should inexorably is typical of lorises, it is accompanied by a host of evolve euprimate‐like traits. This has never been an cranial and postcranial autapomorphies that make it axiom of the angiosperm co‐evolutionary model, possible. Tarsiers employ the opposite strategy as sit‐ though it follows the thrust of Cartmill’s reasoning and‐wait ambush predators and they, too, are [1974]. In any event, such strict adherence to the radically specialized. Incidental gleaning of overt presumption of mirror image convergence among prey and unburying concealed prey does occur across

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the order but without coordinated support from clear‐ explanation of orbital convergence and frontation cut, cross‐system, universal adaptive complexes. [Changizi and Shimojo, 2008] would greatly benefit To wit, the two‐handed prehension patterns of such a system and contribute to the evolution of strepsirhines, tarsiers and marmosets, while quite highly dynamic locomotion. This capacity presup- advanced relative to the “unemancipated” limbs of poses the ability to interpolate and integrate the other mammals, seem primitively awkward in the spread fingers of the hand, branch dimensions, process of snapping up prey. contour, texture, and complex surroundings as the Paleontologically, the case for the small‐eyed, vestibular system learns and calibrates itself via large‐snouted plesiadapiforms being visual preda- visual‐tactile feedback. Similarly, experimental stud- tors is confoundingly prohibitive, even for species ies have suggested various explanations for the whose molars appear to be shaped for insectivory [see postorbital bar, regarding it, on the one hand, as a Silcox et al., 2007a,b]. For omnivorous‐frugivorous cranial strut that facilitates mastication [Ravosa animals, seeds—an archetypical terminal branch et al., 2000] and, on the other, as an attachment site food eaten by an enormous array of small mammals, for eye‐stabilizing ligaments that counteracts the both arboreal and terrestrial—may have provided a effects of mastication [Heesy, 2005]. To extend reliable source of proteins and lipids within the Rosenberger and Preuschoft’s [2012] modeling study vegetation spectrum, less haphazardly and more of the tarsier partial postorbital septum, the bar may cheaply than insects. While some families within the also serve as a stabilizer of the eye under challenging diverse plesiadapiform radiation were probably more locomotor conditions, such as the high g‐force insectivorous [Kay and Cartmill, 1977] and other accelerations and decelerations of leaping. All these advanced forms more folivorous [Boyer et al., 2010], possibilities suggest that absent a more comprehen- the majority of examples drawn from every lineage sive, system‐integrating analysis, it is not possible to surrounding the origins of euprimates (plesiada- determine that stereoscopy was selected solely, or poids, adapiforms, and tarsiiforms) suggest that even preferentially, for roles underlying visual vegetation was the predominant source of PFs and predation as opposed to other behaviors. Inferring SFBFs, as with living primates. the specifics of food type from the cranium requires the Advocates of the visual predation hypothesis rely support of dental evidence, especially when it hy- on non‐dental features said to reflect prey detection pothesizes an exception to the ordinal ecological rule. via stereoscopy: the postorbital bar and convergent eyes of euprimates [e.g., Cartmill, 1992, 2012; Noble et al., 2000; Ravosa et al., 2000]. However, no explicit CONCLUSION connection between the bar and predation is likely to Morphological continuity and adaptive overlap ever be made and the actual perceptual benefits of between crown and stem taxa, and the near stereoscopy are difficult to determine. Nakayama universality of vegetation as today’s core PFs and [2005] maintains stereopsis provides “unambiguous SFBFs, suggests it was also the basal diet of the first information about depth” [p. 6] that triggers aware- recognizable primates as they entered the primate ness of object boundaries, an effect that would benefit adaptive zone. A more precise inference may be canopy locomotion and foraging, among other facul- difficult to square with the power of resolution of ties. Still, if correct, interpreting this aptitude as a gross morphological methods except by exclusion, predatory adaptation suffers from over‐specification that is, by eliminating leaf and insect eating among by presuming a one‐to‐one correspondence between a the most relevant fossils. A thorough re‐evaluation of single physiological function and one of many Paleocene‐Eocene primate diets using modern meth- potential biological roles. Multiple and diverse odologies [see Boyer, 2008], an updated paleontologi- selective benefits may have advantaged early eupri- cal model of primate food choice based on new mates with comparatively close‐set and forward‐ evidence from the living forms, and an approach facing eyes. that emphasizes evolutionary transitions and pread- For instance, experimental evidence [Patla aptation rather than a static morphology would be et al., 2002] has shown that the absence of stereo- most informative [see Silcox et al., 2007a,b]. Today, scopic vision impedes “adaptive” locomotion, espe- the rarity of insects as PFs or SFBFs makes it cially in an object‐filled environment. Modern unlikely that an annual or seasonal diet reliant on primates, if anything, are adaptive locomotors. prey was the predominant driver of selection for Also, the integration of tactile and visual sensory augmented vision as a euprimate or primate univer- systems is often overlooked in discussions of optical sal. The evident coordination of keen eyesight, slicing advances across the primate‐euprimate divide [see cheek teeth and fleet quadrupedalism (among many Yau et al., 2009]. The extent of their interconnected- other attributes) lends a robust measure of credibility ness is easily demonstrated by our own capacity to to the inference that orbital orientation was a central recognize shapes via tactile input under blind element in achieving the carnivoran predatory conditions. The close‐quarters visual acuity and adaptive zone. But it logically faults the visual comprehension emphasized in the “X‐ray vision” predation hypothesis of primate origins, where no

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