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Dental Topographic Change with Macrowear and Dietary Inference in Homunculus Patagonicus

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Dental Topographic Change with Macrowear and Dietary Inference in Homunculus Patagonicus Journal of Human Evolution 144 (2020) 102786 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Dental topographic change with macrowear and dietary inference in Homunculus patagonicus * Peishu Li a, b, c, , Paul E. Morse d, e, Richard F. Kay b, d a Department of Organismal Biology and Anatomy, University of Chicago, Chicago IL, USA b Division of Earth and Ocean Sciences, Nicholas School of the Environment, Duke University, Durham, NC, USA c Department of Biology, Duke University, Durham, NC, USA d Department of Evolutionary Anthropology, Duke University, Durham, NC, USA e Florida Museum of Natural History, University of Florida, Gainesville, FL, USA article info abstract Article history: Homunculus patagonicus is a stem platyrrhine from the late Early Miocene, high-latitude Santa Cruz Received 5 July 2019 Formation, Argentina. Its distribution lies farther south than any extant platyrrhine species. Prior studies Accepted 16 March 2020 on the dietary specialization of Homunculus suggest either a mixed diet of fruit and leaves or a more Available online 11 May 2020 predominantly fruit-eating diet. To gain further insight into the diet of Homunculus, we examined how the occlusal surfaces of the first and second lower molars of Homunculus change with wear by using Keywords : three homology-free dental topographic measures: Dirichlet normal energy (DNE), orientation patch Homunculus count rotated (OPCR), and relief index (RFI). We compared these data with wear series of three extant Dental topography Diet platyrrhine taxa: the folivorous Alouatta, and the frugivorous Ateles and Callicebus (titi monkeys now in Platyrrhini the genus Plecturocebus). Previous studies found Alouatta and Ateles exhibit distinctive patterns of change Paleoecology in occlusal morphology with macrowear, possibly related to the more folivorous diet of the former. Based South America on previous suggestions that Homunculus was at least partially folivorous, we predicted that changes in dental topographic metrics with wear would follow a pattern more similar to that seen in Alouatta than in Ateles or Callicebus. However, wear-induced changes in Homunculus crown sharpness (DNE) and complexity (OPCR) are more similar to the pattern observed in the frugivorous Ateles and Callicebus. Based on similar wear modalities of the lower molars between Homunculus and Callicebus, we infer that Homunculus had a primarily frugivorous diet. Leaves may have provided an alternative dietary resource to accommodate fluctuation in seasonal fruiting abundance in the high-latitude extratropical environ- ment of late Early Miocene Patagonia. © 2020 Elsevier Ltd. All rights reserved. 1. Introduction (Hershkovitz, 1981; Tauber, 1991; Tejedor and Rosenberger, 2008; Kay et al., 2012a; Perry et al., 2014; Novo et al., 2018; Kay and Platyrrhines first appeared in South American Amazonia in the Perry, 2019), and its paleobiology has been extensively studied late Eocene (~31 mya; Bond et al., 2015). By 21 Ma, they had spread (Perry et al., 2010; Ryan et al., 2012; Kay et al., 2012a). Nonetheless, across the continent, with several stem groups appearing at high the diet of Homunculus remains unresolved based on existing cra- latitudes, outside the range of living crown platyrrhines (Kay et al., niodental analyses. Shearing quotient analyses on Homunculus 2012a; Kay, 2015). Among these high-latitude taxa, Homunculus lower first molars suggested either a predominantly frugivorous patagonicus Ameghino (1891) from the Early Miocene Santa Cruz diet (Fleagle et al., 1997) or a mixed diet of fruit and leaves (Kay Formation of Patagonia documents the southern limit of platyr- et al., 2012a). A recent landmark-based morphometric analysis of rhine occurrences (51 S Fig. 1; Kay et al., 2012a). Homunculus is Homunculus upper first molars supports frugivory as well (Kay known from a series of well-preserved cranial, dental, and post- et al., 2019). However, Homunculus is also characterized by un- cranial elements argued to represent at least three species usually heavy postcanine tooth wear, relatively small incisors, and large postcanine tooth root size, all of which are more similar to extant folivorous or durophagous platyrrhines than to frugivores * Corresponding author. (Hylander, 1975; Eaglen, 1984; Spencer, 2003; Perry et al., 2010). E-mail address: [email protected] (P. Li). https://doi.org/10.1016/j.jhevol.2020.102786 0047-2484/© 2020 Elsevier Ltd. All rights reserved. 2 P. Li et al. / Journal of Human Evolution 144 (2020) 102786 Figure 1. Map of South America. Pink area represents the current distributional limits of platyrrhines. Red star denotes location of late Early Miocene fossil localities of Homunculus at ~51 S. Although South America has drifted westward and rotated clockwise since the Early Miocene, the paleolatitude of Patagonia was nearly the same as today. (For inter- pretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) Mandibular corpus depth and articular surface area of the analyses offer alternative means to quantify functionally relevant mandibular condyle suggest repetitive loading during chewing characteristics on molar occlusal surface at different wear stages (Kay et al., 2012a), and small chewing muscle attachment sites and (Ungar and Williamson, 2000; Ungar and M'Kirera, 2003; Evans poor masticatory leverage discount the possibility that Homunculus et al., 2007; Boyer, 2008; Bunn et al., 2011; Winchester et al., was a hard-object feeder (Perry et al., 2010) but do not address the 2014). Some of these metrics include relief index (RFI; Boyer, possibility that it was a folivore. 2008), occlusal relief (Ungar and Williamson, 2000), Dirichlet Both shearing quotient and landmark-based morphometrics normal energy (DNE; Bunn et al., 2011), and orientation patch require careful landmark selection on an unworn or lightly worn count rotated (OPCR; Evans et al., 2007; Evans and Janis, 2014; occlusal surface with defined cusps. Their ability to accurately Pineda-Munoz et al., 2017). Functionally in primates, high- predict diet may therefore be affected by the degree of tooth wear. crowned molars with sharp occlusal surfaces correlate with high Several recently developed homology-free dental topographic RFI, occlusal relief, and DNE values, while higher OPCR correlates P. Li et al. / Journal of Human Evolution 144 (2020) 102786 3 with more complex occlusal surfaces. These metrics are effective at d Smithsonian National Museum of Natural History, Washington assigning extant primates into heuristic dietary groups based on DC, USA. unworn dentitions (Boyer, 2008; Bunn et al., 2011; Winchester et al., 2014) and have been used to infer the dietary ecology of 2.2. Sample and mesh preparation several extinct groups, including Plesiadapiforms (Boyer et al., 2010; Prufrock et al., 2016a; Lopez-Torres et al., 2018), the Twenty-one specimens of Homunculus first (M1) and second ground-dwelling lemur Hadropithecus (Godfrey et al., 2012), the (M2) lower molars (six original fossil specimens and 15 high- fossil colobine Mesopithecus (Thiery et al., 2017), and various extinct fidelity epoxy resin casts) were sampled from the collections of hominins (Berthaume et al., 2018). So far, however, no studies have Museo Argentino de Ciencias Naturales Bernardino Rivadavia, utilized these techniques on fossil platyrrhines (but see Cooke, Museo de La Plata, and Museo Regional Provincial Padre Manuel 2011, for using three-dimensional (3D) morphometrics on fossil Jesús Molina (Table 1). High-fidelity epoxy resin casts of 13 variably platyrrhine mandibular molars to infer paleodiet). worn Callicebus M1 specimens were sampled from the American Most existing dental topography studies have utilized a cross- Museum of Natural History (Callicebus hoffmannsi), Field Museum sectional approach (e.g., Ungar et al., 2018), while longitudinal of Natural History (Callicebus moloch), and Smithsonian Museum of sampling of occlusal morphology across a wear series over an an- Natural History (Callicebus ornatus). All Callicebus specimens imal's lifetime is uncommon, with some exceptions (Dennis et al., included here fall within the moloch group, which was recently 2004; King et al., 2005). Recently, several studies by Pampush placed in the new genus Plecturocebus based on molecular and et al. found that in the folivorous Alouatta Lacep ede, 1799, lower biogeographic data (Table 2; Byrne et al., 2016). However, in this first molar DNE increases linearly with macrowear, while the study, we use the traditional genus name associated with titi closely related frugivorous Ateles Geoffroy Saint-Hilaire, 1806 monkeys d Callicebus d for easier recognition and to maintain maintains consistent DNE values throughout the wear series consistency with accession data in the respective museums from (Pampush et al., 2016a, 2018). These authors inferred that Alouatta, which specimens were sampled. Readers are directed to the study with its more folivorous diet, has teeth adapted to wear via enamel by Byrne et al. (2016) for a thorough review of the taxonomy of sculpting (Ungar, 2015), whereas the more frugivorous Ateles lacks current and previous members of Callicebus. All extant specimen such an adaptation. If tooth wear modalities are indeed diet- data were collected from wild individuals. The number of molars specific in extant primates (i.e., enamel sculpting, Ungar, 2015; studied for each taxon is comparable with
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