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      Dietary Specialization during the Evolution of Western Eurasian Hominoids and the Extinction of European Great Apes

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          Abstract

          Given the central adaptive role of diet, paleodietary inference is essential for understanding the relationship between evolutionary and paleoenvironmental change. Here we rely on dental microwear analysis to investigate the role of dietary specialization in the diversification and extinction of Miocene hominoids from Western Eurasian between 14 and 7 Ma. New microwear results for five extinct taxa are analyzed together with previous data for other Western Eurasian genera. Except Pierolapithecus (that resembles hard-object feeders) and Oreopithecus (a soft-frugivore probably foraging opportunistically on other foods), most of the extinct taxa lack clear extant dietary analogues. They display some degee of sclerocarpy, which is most clearly expressed in Griphopithecus and Ouranopithecus (adapted to more open and arid environments), whereas Anoiapithecus, Dryopithecus and, especially, Hispanopithecus species apparently relied more strongly on soft-frugivory. Thus, contrasting with the prevailing sclerocarpic condition at the beginning of the Eurasian hominoid radiation, soft- and mixed-frugivory coexisted with hard-object feeding in the Late Miocene. Therefore, despite a climatic trend towards cooling and increased seasonality, a progressive dietary diversification would have occurred (probably due to competitive exclusion and increased environmental heterogeneity), although strict folivory did not evolve. Overall, our analyses support the view that the same dietary specializations that enabled Western Eurasian hominoids to face progressive climatic deterioration were the main factor ultimately leading to their extinction when more drastic paleoenvironmental changes took place.

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          Dental microwear texture analysis shows within-species diet variability in fossil hominins.

          Reconstructing the diets of extinct hominins is essential to understanding the paleobiology and evolutionary history of our lineage. Dental microwear, the study of microscopic tooth-wear resulting from use, provides direct evidence of what an individual ate in the past. Unfortunately, established methods of studying microwear are plagued with low repeatability and high observer error. Here we apply an objective, repeatable approach for studying three-dimensional microwear surface texture to extinct South African hominins. Scanning confocal microscopy together with scale-sensitive fractal analysis are used to characterize the complexity and anisotropy of microwear. Results for living primates show that this approach can distinguish among diets characterized by different fracture properties. When applied to hominins, microwear texture analysis indicates that Australopithecus africanus microwear is more anisotropic, but also more variable in anisotropy than Paranthropus robustus. This latter species has more complex microwear textures, but is also more variable in complexity than A. africanus. This suggests that A. africanus ate more tough foods and P. robustus consumed more hard and brittle items, but that both had variable and overlapping diets.
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            Dental enamel as a dietary indicator in mammals.

            The considerable variation in shape, size, structure and properties of the enamel cap covering mammalian teeth is a topic of great evolutionary interest. No existing theories explain how such variations might be fit for the purpose of breaking food particles down. Borrowing from engineering materials science, we use principles of fracture and deformation of solids to provide a quantitative account of how mammalian enamel may be adapted to diet. Particular attention is paid to mammals that feed on 'hard objects' such as seeds and dry fruits, the outer casings of which appear to have evolved structures with properties similar to those of enamel. These foods are important in the diets of some primates, and have been heavily implicated as a key factor in the evolutionary history of the hominin clade. As a tissue with intrinsic weakness yet exceptional durability, enamel could be especially useful as a dietary indicator for extinct taxa.
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              Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus.

              Studies of dental microwear have been used to relate tooth form to function in a variety of recent and extinct mammals. Probably the most important aspect of microwear analysis is the possibility of using it to deduce the diet of extinct animals. Such deductions must be based on comparative studies of modern species with known diets, but to date, only qualitative studies have been attempted and all have been based on small samples. Here we report quantitative differences in dental microwear between primate species that are known to have different diets. Occlusal facets with different functions have previously been shown to exhibit different microwear patterns. However, the differences between facets of one species are shown to be far less than those between homologous facets of different species. Study of seven species of extant primates shows that enamel microwear can be used to distinguish between those with a mainly frugivorous diet and those with a mainly folivorous one. Microwear can also distinguish hard-object feeders from soft-fruit eaters. The microwear of Miocene Sivapithecus indicus cannot be distinguished statistically from that of the chimpanzee, but it is different from that of the other species. On this evidence S. indicus was not a hard-object feeder and the adaptive significance of its thick molar enamel is at present unknown.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                21 May 2014
                : 9
                : 5
                : e97442
                Affiliations
                [1 ]Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain
                [2 ]Dipartimento di Scienze della Terra, Università di Torino, Torino, Italy
                [3 ]ICREA at Institut Català de Paleontologia Miquel Crusafont and Unitat d’Antropologia Biològica (Dept. BABVE), Universitat Autònoma de Barcelona, Barcelona, Spain
                University of Florence, Italy
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DDM DMA SMS. Performed the experiments: DDM. Analyzed the data: DDM DMA. Contributed to the writing of the manuscript: DDM DMA. Generated the figures: DDM.

                Article
                PONE-D-14-12590
                10.1371/journal.pone.0097442
                4029579
                24848272
                87015abf-38a5-4944-a4a8-a6d4907eb644
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 March 2014
                : 14 April 2014
                Page count
                Pages: 13
                Funding
                This work was funded by the Spanish Ministerio de EconomÍa y Competitividad (CGL2011-28681/BTE, CGL2011-27343, JCI-2011-11697 (to DDM), and RYC-2009-04533 (to DMA)) and the Generalitat de Catalunya (2009 SGR 754 GRC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Paleontology
                Paleobiology
                Paleozoology
                Vertebrate Paleontology
                Paleoanthropology
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. Our data may be found within the manuscript and in the supporting information Tables.

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