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Inferring Locomotor Behaviours in Miocene New World Monkeys Using View metadata, citation and similar papersDownloaded at core.ac.uk from http://rsif.royalsocietypublishing.org/ on September 27, 2018 brought to you by CORE provided by Diposit Digital de Documents de la UAB Inferring locomotor behaviours in Miocene New World monkeys using finite rsif.royalsocietypublishing.org element analysis, geometric morphometrics and machine-learning Research classification techniques applied to talar morphology Cite this article: Pu¨schel TA, Marce´-Nogue´ J, Gladman JT, Bobe R, Sellers WI. 2018 Inferring 1 2,3 4 5,6 locomotor behaviours in Miocene New World Thomas A. Pu¨schel , Jordi Marce´-Nogue´ , Justin T. Gladman , Rene´ Bobe monkeys using finite element analysis, and William I. Sellers1 geometric morphometrics and machine- 1 learning classification techniques applied to School of Earth and Environmental Sciences, University of Manchester, Manchester M13 9PL, UK 2Center of Natural History (CeNak), Universita¨t Hamburg, Martin-Luther-King-Platz 3, Hamburg 20146, Germany talar morphology. J. R. Soc. Interface 15: 3Institut Catala` de Paleontologia M. Crusafont, Universitat Auto`noma de Barcelona, Cerdanyola del Valle`s, 20180520. Barcelona 08193, Spain 4 http://dx.doi.org/10.1098/rsif.2018.0520 Department of Engineering, Shared Materials Instrumentation Facility (SMIF), Duke University, Durham, NC, USA 5Departamento de Antropologı´a, Universidad de Chile, Santiago, Chile 6Institute of Cognitive and Evolutionary Anthropology, School of Anthropology, University of Oxford, Oxford, UK Received: 9 July 2018 TAP, 0000-0002-2231-2297; JM-N, 0000-0001-9852-7027; WIS, 0000-0002-2913-5406 Accepted: 28 August 2018 The talus is one of the most commonly preserved post-cranial elements in the platyrrhine fossil record. Talar morphology can provide information about postural adaptations because it is the anatomical structure responsible for transmitting body mass forces from the leg to the foot. The aim of this Subject Category: study is to test whether the locomotor behaviour of fossil Miocene platyr- Life Sciences–Engineering interface rhines could be inferred from their talus morphology. The extant sample was classified into three different locomotor categories and then talar Subject Areas: strength was compared using finite-element analysis. Geometric morpho- metrics were used to quantify talar shape and to assess its association biomechanics, evolution, with biomechanical strength. Finally, several machine-learning (ML) algor- computational biology ithms were trained using both the biomechanical and morphometric data from the extant taxa to infer the possible locomotor behaviour of the Mio- Keywords: cene fossil sample. The obtained results show that the different locomotor Platyrrhini, finite-element modelling, categories are distinguishable using either biomechanical or morphometric morphometrics, talus, statistical learning, data. The ML algorithms categorized most of the fossil sample as arboreal positional behaviour quadrupeds. This study has shown that a combined approach can contribute to the understanding of platyrrhine talar morphology and its relationship with locomotion. This approach is likely to be beneficial for determining the locomotor habits in other fossil taxa. Author for correspondence: Thomas A. Pu¨schel e-mail: [email protected] 1. Introduction Extant platyrrhines or New World monkeys (NWM) inhabit a diverse range of habitats in the Americas [1]. The occupation of these niches has been coupled by distinct behavioural, locomotor, morphological and ecological adaptations in each one of the main platyrrhine clades [2], which can be summarized in broad ecophyletic groups (figure 1). One of the main difficulties in NWM palaeobiology is the scarceness of fossils from the Eocene and Oligocene, Electronic supplementary material is available with most NWM fossils dated to the Miocene or the Pleistocene of the Carib- online at https://dx.doi.org/10.6084/m9. bean and South America [3], although it is important to note that there have figshare.c.4219997. & 2018 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from http://rsif.royalsocietypublishing.org/ on September 27, 2018 clamber/suspensory 2 arboreal quadruped leaper rsif.royalsocietypublishing.org dentition- dentition- durophagy sclerocarpy encephalization ancestral platyrrhine J. R. Soc. Interface diet: frugivory/insectivory locomotion: arboreal Cebinae quadruped/leaper Pitheciidae diet: omnivory/frugivory size: small/medium size diet: seed predation locomotion: arboreal quadruped locomotion: canopy dwellers - arboreal suspensory locomotion size: ~750–3500 g quadruped tail assisted nocturnal- size: ~750–4000 g cathemeral 15 al locomotion : 20180520 miniature sizeclaws scansori Callitrichinae Aotinae Atelidae diet: diet: primarily frugivorous diet: frugivory/folivory frugivory/exudativory/insectivory locomotion: arboreal quadruped locomotion: climber/clamber locomotion: clawed/leaper size: ~700–1200 g suspensory behaviours size: ~100–700 g size: ~5000–14 000 g Figure 1. Broad platyrrhine ecophyletic groups. Colours represent different main locomotion modes. (Online version in colour.) been outstanding but rare findings in Bolivia and Peru [4]. biomechanical performance as a positional behaviour proxy Even though the fossil record of NWM has notably improved [12]. Consequently, we analysed the biomechanical perform- over the last decade, it is particularly intriguing that the ance of the extant platyrrhine talar morphological diversity majority of the NWM fossil record for the Early Miocene by applying finite-element analysis (FEA). There is an has been found in middle and high latitudes (i.e. central almost total absence of studies applying FEA to primate, Chile and Patagonia), which are no longer areas occupied let alone platyrrhine, talar biomechanics. To our knowledge, by any extant platyrrhine [5]. most studies analysing primate talar biomechanics using FEA After teeth, the talus is probably the most commonly have focused on human feet (e.g. [13–15]). Thus, the present preserved anatomical element in the platyrrhine fossil contribution represents an important step in analysing an record [3], with several Miocene taxa possessing at least extensive non-human primate comparative sample using one conserved talus [6]. Importantly, talar morphology can FEA. Since we were also interested in the relationship provide insights about postural adaptations due to its inter- between talar biomechanical performance and its mor- connection with other foot bones [7,8]. The talus is also phology, we used geometric morphometrics (GMs) to the principal mechanical connection between the leg and collect shape data. In addition, because our objective was to the foot and is responsible for transmitting body weight, classify the fossils into different locomotor categories, several as well as providing stability and mobility throughout machine-learning (ML) algorithms were trained using the locomotor behaviours [7]. The combination of its high occur- extant biomechanical data to infer the locomotor categories rence and good preservation in the fossil record and its of the Miocene fossil sample. Traditionally, most morpho- functional role in the ankle joint make it a valuable element metric and also some of the FEA output analyses have been when hypothesizing the postural and locomotor behaviours performed with reference to simple linear models [16,17]. of fossil primates [9,10]. For instance, when dealing with classification problems, There is a strong and significant association between talar most publications rely on linear discriminant analyses (or shape and locomotor behaviour [6], and evidence shows that its more general extension, canonical variate analyses), in bone is functionally adapted to the mechanical demands that spite of the known limitations of these approaches [18,19]. are imposed during life [11]. Therefore, it is logical to hypoth- Although the application of ML algorithms to tackle pro- esize that talar mechanical strength associated with blems of specimen identification or group characterization biomechanical performance could also be used to distinguish has a vast literature in other biological fields [20], only and infer locomotor behaviours. Currently, there is an more recently have several ML methods been applied using absence of comparative biomechanical analyses that could morphometric or biomechanical data (e.g. [13–15,21–26]). provide important information about the usefulness of talar In addition, most of them have not compared different Downloaded from http://rsif.royalsocietypublishing.org/ on September 27, 2018 algorithms applied to the same problem. Therefore, some of 2.3. Finite-element analysis 3 these ML procedures were explored and their classification w The models of the tali were imported into ANSYS (Ansys, Inc., rsif.royalsocietypublishing.org accuracy was assessed when applied to the problem of classi- v. 17.1, Canonsburg, PA, USA; http://www.ansys.com/) to per- fying our Miocene fossil sample using morphometric and form the FEA modelling. The tali were modelled as solids biomechanical data. composed only of cortical bone to simplify the analyses and to Consequently, this study had three main aims for which limit the number of assumptions. Homogeneous, linear and elas- we employed three different approaches. (i)
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