Limitations of a morphological criterion of adaptive inference in the fossil record

Experimental analyses directly inform how an anatomical feature or complex functions during an organism's lifetime, which serves to increase the efficacy of comparative studies of living and fossil taxa. In the mammalian skull, food material properties and feeding behaviour have a pronounced influence on the development of the masticatory apparatus. Diet-related variation in loading magnitude and frequency induce a cascade of changes at the gross, tissue, cellular, protein and genetic levels, with such modelling and remodelling maintaining the integrity of oral structures vis-à-vis routine masticatory stresses. Ongoing integrative research using rabbit and rat models of long-term masticatory plasticity offers unique insight into the limitations of functional interpretations of fossilised remains. Given the general restriction of the palaeontological record to bony elements, we argue that failure to account for the disparity in the hierarchical network of responses of hard versus soft tissues may overestimate the magnitude of the adaptive divergence that is inferred from phenotypic differences. Second, we note that the developmental onset and duration of a loading stimulus associated with a given feeding behaviour can impart large effects on patterns of intraspecific variation that can mirror differences observed among taxa. Indeed, plasticity data are relevant to understanding evolutionary transformations because rabbits raised on different diets exhibit levels of morphological disparity comparable to those found between closely related primate species that vary in diet. Lastly, pronounced variation in joint form, and even joint function, can also characterise adult conspecifics that differ solely in age. In sum, our analyses emphasise the importance of a multi-site and hierarchical approach to understanding determinants of morphological variation, one which incorporates critical data on performance

Problems with paranthropus

Carbon isotopic analysis has been challenging our ideas about hominin diet for nearly 30 years. The first study in 1994 revealed that Paranthropus robustus from South Africa consumed principally C3 foods (e.g., tree fruits and leaves) but also about 25% C4/CAM resources (e.g., tropical grasses and sedges). This result was largely consistent with morphological and dental microwear evidence suggesting P. robustus had a diet which included hard objects like nuts and seeds. Decades later, however, P. boisei from eastern Africa was shown to have eaten nearly 80% C4/CAM plants like the contemporaneous grass-eating primate Theropithecus. Moreover, dental microwear revealed no evidence of hard object consumption in P. boisei, suggesting a diet of tough foods such as grass or sedge leaf and stem. So Paranthropus presents us with two central problems: 1) Why do dietary proxies suggest different diets for the two robust australopiths despite their morphological congruity; and 2) How could P. boisei have consumed tough foods with teeth that seem unsuited to the task. Here we review these questions and more with a particular focus on new isotopic data from the Omo and insights that can be gleaned from mammals outside the haplorrhine primates. We argue that extant Primates do not capture the ecomorphological diversity of P. boisei and other extinct primates and should not narrowly circumscribe the behaviors we ascribe to extinct taxa. We also discuss possible digestive strategies for P. boisei in light of its morphology, dietary proxy data, food mechanical properties, and comparative data on mammalian digestive kinetics.info:eu-repo/semantics/publishedVersio

Hard-Object Feeding in Sooty Mangabeys (Cercocebus atys) and Interpretation of Early Hominin Feeding Ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods

Morphologie fonctionnelle, biomécanique et rétrodiction du régime alimentaire des premiers homininés

Un axiome fondamental sous-jacent à l’analyse évolutive de la biomécanique soutient que la sélection naturelle a permis les adaptations du squelette et des dents en facilitant leur fonction de manière intelligible. Puisque la sélection sous-tend à améliorer le patron fonctionnel, il est généralement estimé possible de prédire la valeur adaptative d’une caractéristique morphologique à partir d’un modèle. Ce raisonnement a été largement appliqué pour interpréter des complexes morphologiques dans le registre paléontologique pour lequel il n’existe pas d’équivalents actuels. En particulier, les modèles biomécaniques ont été utilisés pour déduire les habitudes alimentaires des taxons homininés éteints à partir de la morphologie cranio-dentaire. Nombre de ces modèles sont limités par des données manquantes et des suppositions vaguement justifiées. La morphologie cranio-dentaire peut vraisemblablement nous renseigner davantage sur les capacités d’un taxon éteint à traiter les aliments dans sa cavité buccale – et probablement plus encore sur son histoire phylogénétique – que sur la constitution de son régime alimentaire. Même un homininé spécialisé dans une alimentation folivore n’a pas forcément des molaires bilophodontes. La rétrodiction du régime alimentaire basée sur l’anatomie comparée telle qu’elle a été appliquée aux taxons homininés plio-pléistocènes est examinée ici. Nous discutons le fait que l’application d’analyses par éléments finis à ces fossiles n’a pas révélé d’éléments convaincants concernant des habitudes alimentaires particulières. En effet, les conclusions basées sur ces modèles biomécaniques sont souvent contradictoires avec les données issues de l’analyse des isotopes stables légers, des micro-usures et des phytolithes, et ne sont pas non plus compatibles avec les observations sur les répertoires alimentaires et les habitudes de nutrition des primates actuels. Par exemple, le mangabey couronné (Cercocebus atys) est spécialisé dans la consommation d’aliments durs, mais ne souffre aucunement de la « faible constitution » de son squelette facial pour mastiquer de la nourriture dure. Parce que les primates sont des experts pour contourner de manière comportementale des problèmes biomécaniques, il serait peut-être utile de considérer l’ensemble des possibilités du répertoire alimentaire de chaque homininé dans un contexte comportemental qui inclut la possibilité de faire face aux problèmes biomécaniques avant ingestion.A fundamental axiom that underlies evolutionary biomechanics maintains that natural selection has adapted skeletal and dental morphologies to facilitate function in intelligible ways. Because selection is held to result in the improvement of functional design, it is thought possible to predict the adaptive significance of a morphological feature from a design criterion. This rationale has been widely applied to the interpretation of morphological complexes in the paleontological record for which no strict extant analogues exist. In particular, biomechanical models have been used to infer the dietary habits of extinct hominin taxa from aspects of craniodental morphology. Many of these models are hampered by missing data and loosely justified assumptions. Craniodental morphologies may indicate more about what an extinct species was capable of processing intra-orally – and probably more about its phylogenetic history – than the constitution of its diet. Even a dedicated leaf-eating hominin cannot be expected to have possessed bilophodont molars. The dietary retrodictions based on comparative anatomical that have been proffered for Plio-Pleistocene hominin species are reviewed here. We argue that the application of finite element analysis to these fossils has not revealed convincing evidence of specific feeding behaviors. Indeed, the conclusions from these biomechanical models are often incongruent with data from stable light isotopes, microwear and phytolith analysis; nor do they conform with observations on the dietary repertoires and feeding behaviors of extant primates. For example, the sooty mangabey (Cercocebus atys) is a committed hard object feeder, but suffers no deleterious consequences from the “poor design” of its facial skeleton for processing hard foods. Because primates are adept at behaviorally circumventing mechanical problems, it is perhaps useful to consider the breadth of any fossil hominin\u27s feeding repertoire in the context of behaviors that enable mechanical problems to be dealt with prior to ingestion.</p

Viewpoints: Feeding mechanics, diet, and dietary adaptations in early hominins

Inference of feeding adaptation in extinct species is challenging, and reconstructions of the paleobiology of our ancestors have utilized an array of analytical approaches. Comparative anatomy and finite element analysis assist in bracketing the range of capabilities in taxa, while microwear and isotopic analyses give glimpses of individual behavior in the past. These myriad approaches have limitations, but each contributes incrementally toward the recognition of adaptation in the hominin fossil record. Microwear and stable isotope analysis together suggest that australopiths are not united by a single, increasingly specialized dietary adaptation. Their traditional (i.e., morphological) characterization as "nutcrackers" may only apply to a single taxon, Paranthropus robustus. These inferences can be rejected if interpretation of microwear and isotopic data can be shown to be misguided or altogether erroneous. Alternatively, if these sources of inference are valid, it merely indicates that there are phylogenetic and developmental constraints on morphology. Inherently, finite element analysis is limited in its ability to identify adaptation in paleobiological contexts. Its application to the hominin fossil record to date demonstrates only that under similar loading conditions, the form of the stress field in the australopith facial skeleton differs from that in living primates. This observation, by itself, does not reveal feeding adaptation. Ontogenetic studies indicate that functional and evolutionary adaptation need not be conceptually isolated phenomena. Such a perspective helps to inject consideration of mechanobiological principles of bone formation into paleontological inferences. Finite element analysis must employ such principles to become an effective research tool in this context. © 2013 Wiley Periodicals, Inc

Oral Processing of Three Guenon Species in Ta&iuml; National Park, C&ocirc;te d&rsquo;Ivoire

Three guenon species in Ta&iuml; National Park frequently form and maintain stable polyspecific associations despite significant feeding competition. This dietary overlap provides an opportunity to examine how closely related and anatomically similar taxa process the same foods. Our research examines whether the oral-processing behaviors of these guenons differ when they consume the same foods. Methods: Data on oral-processing behavior were collected on one habituated group each of Cercopithecus campbelli, C. diana, and C. petaurista in Ta&iuml; National Park, C&ocirc;te d&rsquo;Ivoire from January 2016 to December 2018. We recorded the frequency with which foods were introduced to the mouth (ingestive action) and the frequency with which foods were processed using incisors, canines, and postcanine teeth. Oral-processing profiles for species-specific plant foods, fungi, and invertebrates were compared using Monte Carlo resampling. We quantified oral-processing behavior during a total of 2316 five-minute focal periods. Diana monkeys use their incisors significantly more per ingestive action than Campbell&rsquo;s monkeys or Lesser spot-nosed guenons. Lesser spot-nosed guenons use their incisors more than Campbell&rsquo;s monkeys. Diana monkeys also use significantly more post-canine chews per ingestive action than Campbell&rsquo;s monkeys and Lesser spot-nosed guenons. Lesser spot-nosed guenons generally use fewer post-canine chews than Diana monkeys but more than Campbell&rsquo;s monkeys. Canine use during feeding was rare in all three taxa. The three study species use different oral-processing profiles when consuming the same foods. These results are intriguing given the overall similarity in dental and cranial anatomy in these taxa. The oral-processing profiles we report do not encompass the full dietary breadth of all species; however, the behavioral diversity demonstrated during consumption of the same foods suggests that insight into feeding behavior is more likely obtained by examining oral processing of individual foods rather than broad food categories. Furthermore, these results underscore that important variation in feeding behavior is not necessarily associated with morphological differences in dental or craniofacial anatomy