Parvimico Materdei Gen. Et Sp. Nov.: a New Platyrrhine from the Early Miocene of the Amazon Basin, Peru11this Publication Has Be

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Journal of Human Evolution 134 (2019) 102628

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Journal of Human Evolution

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Parvimico materdei gen. et sp. nov.: A new platyrrhine from the Early Miocene of the Amazon Basin, Peru1

* Richard F. Kay a, b, , Lauren A. Gonzales c, Wout Salenbien b, Jean-Noel€ Martinez d, Siobhan B. Cooke e, Luis Angel Valdivia d, Catherine Rigsby f, Paul A. Baker b a Department of Evolutionary Anthropology, Box 90383, Duke University, Durham NC 27708, USA b Nicholas School of the Environment, Division of Earth and Ocean Sciences, Duke University, Durham, NC 27708, USA c Biomedical Sciences, University of South Carolina, School of Medicine, Greenville, SC 29605, USA d Instituto de Paleontología, Universidad Nacional de Piura, Campus Universitario, Av. Caceres s/n, Urb. Miraﬂores, Castilla, Piura, Peru e The Center for Functional Anatomy and Evolution, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA f Department of Geological Sciences, East Carolina University, Greenville, NC, USA article info abstract

Article history: Three field seasons of exploration along the Río Alto Madre de Dios in Peruvian Amazonia have yielded a Received 20 November 2018 fauna of micromammals from a new locality AMD-45, at ~12.8S. So far we have identified the new Accepted 31 May 2019 primate described here as well as small caviomorph rodents, cenolestoid marsupials, interatheriid Available online xxx notoungulates, xenarthrans, fish, lizards and invertebrates. The site is in the Bala Formation as exposed Dataset link: https://doi.org/10.17632/ where the river transects a syncline. U-Pb dates on detrital zircons constrain the locality's age at between 66p3c4xzkj.1 17.1 ± 0.7 Ma and 18.9 ± 0.7 Ma, making the fauna age-equivalent to that from the Pinturas Formation and the older parts of the Santa Cruz Formation of Patagonian Argentina (Santacrucian). The primate 1 Keywords: specimen is an unworn M of exceptionally small size (equivalent in size to the extant callitrichine, Anthropoidea Callithrix jacchus, among the smallest living platyrrhines and the smallest Eocene-Early Miocene plat- Platyrrhini yrrhine yet recorded). Despite its small size it is unlike extant callitrichines in having a prominent Paleobiology cingulum hypocone. Based on the moderate development of the buccal crests, this animal likely had a Paleobiogeography diet similar to that of frugivorous callitrichines, and distinctly different from the more similarly-sized South America gummivores, Cebuella and C. jacchus. The phyletic position of the new taxon is uncertain, especially given the autapomorphic character of the tooth as a whole. Nevertheless, its unusual morphology hints at a wholly original and hitherto unknown Amazonian fauna, and reinforces the impression of the geographic separation of the Amazonian tropics from the more geographically isolated southerly parts of the continent in Early Miocene times. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction These river basins were broadly interconnected until the mid- Miocene, and have presumably shared a regional fauna since at Extant platyrrhine primates inhabit a wide range of habitats in least the later Eocene (~40 Ma; Albert et al., 2006). subtropical and tropical forests. The largest number of sympatric The primate fossil record in the tropics and subtropics, where species inhabit Amazonian rainforests with richness up to 16 spe- one would expect this platyrrhine diversification to have occurred, cies (Kay et al., 1997). The present tropical and subtropical Amazon, is exceedingly sparse from the Late Eocene to Middle Miocene (a Orinoco, and Magdalena river basins share a total area of 8.65 timespan of nearly 30 Myr). To date, the total available fossil record million km2, roughly 41% of the total area of continental South of pan-Amazonian monkeys is as follows: 1) two (?) isolated teeth America, and account for 91% of the specific and generic richness of from Late Eocene or Early Oligocene Perupithecus from Santa Rosa, the Platyrrhinid155 species and 21 genera (Estrada et al., 2017). Peru (Bond et al., 2015; Kay, 2015a); 2) many jaws and teeth of Late Oligocene Branisella from Salla, Bolivia (Hoffstetter, 1969; Takai et al., 2000; Kay et al., 2002);2 3) two upper molars of * Corresponding author. E-mail address: [email protected] (R.F. Kay). 1 This publication has been registered in ZooBank (http://zoobank.org) with the 2 Late Oligocene Branisella boliviana comes from Salla, Bolivia in the Cordillera following Life Science Indentifier: lsid:D881BC80-AAB7-4A90-AE8C- Real 4000 m asl, but at the time of its deposition was close to sea level (Garzione 08CAA6981FCE. et al., 2008) and on the periphery of what now is the Amazon Basin. https://doi.org/10.1016/j.jhevol.2019.05.016 0047-2484/© 2019 Elsevier Ltd. All rights reserved. 2 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

Canaanimico from the Late Oligocene of Contamana, Peru (Antoine Machines Analyte G2 excimer laser, feeding into an Element2 HR et al., 2016; Marivaux et al., 2016a); and 4) a single small primate ICPMS to sequence U, Th and Pb isotopes. Data reduction and astragalus from a locality along the Alto Madre de Dios, close by the final age computation was performed with a Python script and locality from which comes the new primate described here the E2agecalc application that is developed in-house at the (Marivaux et al., 2012). Arizona LaserChron Center. Kernel density estimation (KDE) plots It is not until the Middle Miocene (13 Ma and younger) that the of the detrital zircon age distributions were created using the R- record of primates from the tropics becomes more abundant. At La based statistical provenance package (R Core Team, 2016; Venta, Colombia (then continuous with the Amazon-Orinoco ba- Vermeesch et al., 2016) with equal bandwidth for all samples, sins; Hoorn et al., 1995), at least eight Middle Miocene primate and displayed on a logarithmic scale. Sedimentary sources are genera are recorded, representing all three extant families (Kay, based on the orogenic provinces reported by Bahlburg et al. 2015b). At least three other primate taxa have been found in the (2011) and references therein. Maximum depositional ages were Middle and Late Miocene of Amazonia (Kay and Cozzuol, 2006; calculated based on the youngest statically coherent age Marivaux et al., 2016b). population if multiple ages were present, otherwise youngest The majority of the pre-Pleistocene platyrrhine record is located single grain (YSG) ages were used if they could be corroborated peripheral to the tropics. This includes numerous taxa from the by other independent age constraints. Details of the sample Early Miocene of Chile, Argentina, Panama, and Cuba (Flynn preparation, age determination of the rock samples and outcrop et al.,1995; Fleagle and Tejedor, 2002; MacPhee et al., 2003; Kay, descriptions are presented in Mendeley Supplementary Online 2015a; Bloch et al., 2016). The extratropical distribution of these Material available at Mendeley Data (https://doi.org/10.17632/ primates and the fragmentary nature of most of the finds has led to 66p3c4xzkj.1). substantial disagreement about the mode and tempo of platyrrhine evolutiondsome arguing for early divergence of the living families 2.3. Phylogenetic analysis (e.g., Rosenberger, 2010) while others see successive radiations, not stasis (Hodgson et al., 2009; Kay and Fleagle, 2010). To assess the phylogenetic position of IPVF-5000, we employed In short, an improved record for Miocene Amazonian primates, the morphological character-taxon matrix of Kay (2015a), accepting where modern diversity is at its highest and early platyrrhine several modifications of characters of the upper dentition proposed diversification is presumed to have centered, is critical to under- by Marivaux et al. (2016a), and with the addition of the newly standing the evolution of the group in South America. This is described taxa Panamacebus, Canaanimico, and Perupithecus,as underscored by recent molecular clock evidence that places clad- Marivaux et al. (2016a) have done. For this purpose, we evaluated ogenesis of the extant platyrrhine families Pitheciidae, Atelidae, the scoring of the three above-mentioned genera from casts and and Cebidae in greater Amazonia between ~25 and 16 Ma (Jameson descriptions. Additionally, we added substantial new information Kiesling et al., 2015). about Patagonian Miocene platyrrhines based upon undescribed Here, we describe the upper first molar of a new Early Miocene material of Carlocebus and Homunculus.3 platyrrhine primate from Amazonia, in the region of Río Alto Madre The revised character/taxon matrix under consideration con- de Dios and place it within its geological context. We also evaluate sists of 417 characters and 48 taxa, including 19 living genera (16 its phylogenetic position and its ecological niche, especially its body platyrrhines and 3 catarrhines) and 29 fossil taxa (5 Late Eocene- size and diet. Although fragmentary, the specimen, by its small size Oligocene African taxa and 24 ?Late Eocene-Pleistocene platyr- and unusual autapomorphies hints that a much greater radiation of rhines). Some multistate characters are ordered and some unor- stem platyrrhines was ongoing in Amazonia at this time. dered following Kay (2015a) and Marivaux et al. (2016a). Ordered multistate characters were scaled by the number of character 2. Materials and methods states, such that the sum of the steps in the morphocline equals 100. Character descriptions and weights and a NEXUS file is pro- 2.1. Studied specimen vided in SOM S2 and File S1, respectively. All characters and living and fossil taxa were included in the The described specimen (IPVF-5000) is stored in the permanent phylogenetic analysis. The analysis was constrained using a mo- collections of the Instituto de Paleontología e Vertebrados Fosiles, lecular scaffold as recommended by Springer et al. (2001); see Kay Universidad Nacional de Piura, Piura, Peru. Both this publication (2015a) for further discussion. The molecular scaffold is based on a and the new taxa erected herein are registered in ZooBank and the highly corroborated phylogeny of living platyrrhines and catar- resulting life science identifiers (LSID) are provided. The specimen rhines (Jameson Kiesling et al., 2015) with one exception. Jameson- scans were generated at Duke University in the Shared Materials Kiesling et al. (2015) argued that Aotus is sister to Callitrichinae, Instrumentation Facility (SMIF) with a Nikon XTH 225 ST mCT with Cebinae as the outgroup. However, Valencia et al. (2018) scanner with a voltage of 150 kv and an amperage of 65 ma. Voxels highlighted the problematic position of Aotus within the Cebidae are cubic with a resolution of 5.5498 mm. CT images were processed and expressed uncertainty related to possible incomplete lineage using the visualization software Avizo 9.1 (FEI Visualization Sci- sorting and/or ancestral gene flow among the cebid subfamilies ences Group, Berlin, Germany). The surface file (https://doi.org/10. early in the family's history. To express this uncertainty, Aotus is left 17602/M2/M75893) is available for download at Morphosource.org. in a trichotomy with Callitrichinae and Cebinae. Woods et al. (2018) recovered ancient DNA from the extinct Caribbean primate Xeno- 2.2. Radiometric dating thrix and showed that it is most closely related to Callicebus (Cheracebus) lugens. Therefore, we added Xenothrix to our molec- Sample preparation and age determination of samples Zircon ular scaffold giving the revised molecular scaffold: ((((Aotus, samples were prepared and analyzed at the Arizona LaserChron (Saguinus,(Leontopithecus,(Callimico,(Cebuella, Callithrix)))), Center, with only the number of total grains analyzed per sample (Cebus, Saimiri)), (Alouatta,(Ateles,(Brachyteles, Lagothrix)))), being different. U-Pb age determinations of the detrital zircons were conducted following the methods described in Gehrels and Pecha (2004) and Gehrels et al. (2008), through laser ablation 3 We regard Kilikaike Tejedor et al., 2006 to be the subjective junior synonym of coupled plasma mass spectrometry (LA-ICP-MS), using a Photon Homunculus Ameghino, 1891, as explained by Perry et al. (2014). R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 3

((Callicebus, Xenothrix), (Pithecia,(Cacajao, Chiropotes)))), (Hylo- Four separate landmark sets were used in the initial exploratory bates,(Miopithecus, Presbytis))). analyses; landmark set 1 included 8 occlusal landmarks, and The phylogenetic analysis was performed with PAUP 4.0a for landmark set 2 included 11 occlusal landmarks. Landmark sets 3 Macintosh™ (Swofford, 2018), with 1000 replications, using a (16 landmarks) and 4 (23 landmarks) both included sidewall heuristic search with random taxon input, tree-bisection- landmarks. Landmark sets 1 and 3 were used to analyze species reconnection option for branch swapping options. The following from all platyrrhine subfamilies. Landmark sets 2 and 4 included indices were computed: consistency index (CI), retention index landmarks associated with the hypocone and were used to (RI), rescaled consistency index (RC). analyze all platyrrhines except the callitrichines, which largely lack this cusp. The fossil platyrrhines were included in analyses 2.4. Paleobiology using both landmark sets. While landmark set 3 and set 4 provided additional information about sidewall morphology, Body size estimation Body mass was reconstructed from upper dietary reconstruction analyses using these data did not differ molar area using published primate equations by Egi et al. (2004). substantially from the landmark analyses which maximized the Molar area was calculated as buccolingual breadth times number of species; consequently, only results from landmark set mesiodistal width, with measurements taken digitally in Avizo 1 are presented here (for additional details and analyses, see SOM 9.1 (FEI Visualization Sciences Group, Berlin, Germany). Resulting S3). body mass estimates were corrected for logarithmic Landmark data were aligned to minimize the least-squared transformation bias by applying Smith's (1993) ratio estimator distance between landmarks using generalized Procrustes anal- (RE) correction method (see also Snowdon, 1991). RE is calculated ysis (GPA) in Morphologika (O'Higgins and Jones, 2006). GPA- as the arithmetic mean of the observed data divided by the mean alignment brings all of the coordinate landmarks into the same predicted data. The correction is then applied by multiplying the shape space so that further statistical analyses can be performed. predicted body mass by the RE. Principal component analysis (PCA) was performed on the GPA- Diet reconstruction using shearing quotients To reconstruct diet, a aligned landmark points in PAST (Hammer et al., 2001)to new version of the upper first molar shearing quotient (SQ) was examine molar shape of the new specimen relative to extant calculated, which is intended to provide a simplified measure of platyrrhines with a specific focus on functionally significant shape molar cutting edge development. Extant platyrrhine M1 shearing differences. Principal component scores have been previously data were taken from Allen et al. (2015) and expanded to include shown to correlate with platyrrhine diet (Cooke, 2011) and are used additional measurements for 6 genera of small-bodied here for this purpose. callitrichines. The lengths of shearing crests 1 through 4 and Combined shearing quotient and landmark analysis Discriminant mesiodistal tooth lengths (and breadths, reported elsewhere) function analysis (DFA) is generally used to identify which variables were measured one of two ways: under a binocular microscope best discriminate among groups, but also can be used to classify fitted with a reticle eyepiece at 25 magnification, with ungrouped individuals in a sample (Hammer and Harper, 2006). This measurements first taken in reticle units and later converted to makes it a useful technique for classifying fossil specimens for which millimeters, or from 3D surface files using the visualization information is missing. The technique, however, forces each software Avizo 9.1. ‘Total shear’ was then calculated as the sum of shear crest lengths 1 through 4. An SQ reference line was Table 1 calculated by fitting a phylogenetically-corrected least squares Sample of upper first molars used in landmark analyses. (PGLS) regression line to a bivariate plot of natural log mean M1 ‘total shear’ regressed against the natural log of mean M1 Family Species n mesiodistal length for the 11 predominantly frugivorous or Extant sample gumnivorous genera in the sample: Aotus, Ateles, Cacajao, Atelidae Alouatta palliata 7 Callicebus, Callithrix, Cebuella, Cebus, Chiropotes, Lagothrix, Alouatta seniculus 4 Lagothrix lagotricha 9 Leontopithecus, and Pithecia. The branch lengths and topology of Brachyteles arachnoides 9 the tree follows that of Opazo et al. (2006). The derived linear Ateles geoffroyi 9 equation was used to generate an ‘expected’ shearing crest length Cebidae Aotus vociferans 9 for molar length. The expected value was then subtracted from Cebus capucinus 9 Saimiri boliviensis 9 the observed value and divided by the expected value. The Callimico goeldii 9 resultant (SQ value) is expressed here as a percentage. Tooth size Callithrix argentata 5 and shearing development for extant platyrrhine frugivores (by Callithrix jacchus 1 genus) are reported in SOM Table S1 (CSV file). The Nexus file Saguinus labiatus 7 with branch lengths for PGLS and the R-code for the PGLS run are Cebuella pygmaea 4 Pitheciidae Callicebus cupreus 6 provided in SOM Files S2 and S3, respectively. Callicebus moloch 4 Molar shape—landmark analysis Landmark analyses (see review in Pithecia irrorata 9 Adams et al., 2004) of upper first molars were carried out on Cacajao calvus 10 samples of 128 extant and 22 extinct platyrrhine specimens, Chiropotes satanas 8 Extinct Platyrrhini including the holotype of the new species (Table 1). Three- Parvimico materdei 1 dimensional coordinate landmarks were placed on major Soriacebus adrianae 1 anatomical features on the occlusal surface such as cusp tips, Soriacebus ameghinorum 2 basin low points, and the intersection of shearing crests (Fig. 1)to Homunculus patagonicus 3 capture the overall shape of the tooth. For some fossil specimens, Carlocebus carmanensis 3 Neosaimiri fieldsi 4 including the species described here, there was some abrasion or Antillothrix bernensis 2 fracture of the cusp tips. Landmarks were placed at the center of Panamacebus transitus 1 the abraded area. While this damage does affect landmark Insulacebus toussaintiana 1 analyses, fossil specimens were only included if damage was Paralouatta varonai 3 Xenothrix mcgregori 1 limited to one cusp. Damaged extant specimens were excluded. 4 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

3. Geological background and age

3.1. General setting

The geologic section containing the new fossil-bearing locality is situated in the Sub-Andean Zone of the Madre de Dios foreland basin, forming a part of the Eastern Cordillera. The Salvacion Syn- cline and Pantiacolla Anticline are the two main tectonic features in the upper Madre de Dios river valley (Fig. 2). They were produced by tectonic shortening accommodated by the nearby Madre de Dios Detachment Fault that separates the relatively undeformed Amazonian foreland to the east from the actively deforming and eastward-advancing Andes to the west (Louterbach et al., 2014, and references therein). The Salvacion Syncline is asymmetric, with the western ﬂank dips from 80 to subvertically, whereas the eastern ﬂank is characterized by more gently southwest-orientated dips of 30e45 (Vílchez and Hipolito Romero, 1998). Based on sedimentary features and geologic age (from radiometric determinations and fossil content), the outcrop of interest here is assignable to the Bala Formation (Roddaz et al., 2010).

3.2. AMD-45 outcrop and fossil site

The AMD-45 locality (Fig. 2B) is situated on the left bank of the river approximately 10.1 km downstream from the village of Atalaya and 7.6 km downstream from another fossil locality, MD-61, containing a primate astragalus described by Marivaux et al (2012;seeFig. 2C). Both localities are on the western flank of the Salvacíon Syncline where the beds are dipping at 75e80. Fossils, generally in a fragmentary condition, including the pri- Figure 1. Rendering of the CT-scan generated 3D model of IPVF-5000 in occlusal view showing the landmarks used in shape and dietary analyses. Landmarks 3 and 8 (on the mate molar described in this paper, come from the 18e19 m level of hypocone and at the terminus of the prehypocrista) are referenced here for the AMD-45 outcrop, consisting of a conglomerate bed (Fig. 2D). completeness, but were only used in analyses provided in SOM S2. Identification of Bulk sediment was removed from the locality in bags and trans- ¼ ¼ ¼ landmarks: 1 apex of paracone; 2 apex of protocone; 3 apex of hypocone; ported to a nearby site for screen-washing. In total, the amount of 4 ¼ apex of metacone; 5 ¼ mesial interproximal facet; 6 ¼ distal and proximal facet; 7 ¼ deepest point of talon basin; 8 ¼ terminus of the prehypocrista; 9 ¼ junction of material screen-washed from this site was between 800 and postparacrista and premetacrista; 10 ¼ deepest point of trigon basin. 1200 kg. The screening mesh sizes and design follows that described by Cifelli et al. (1996). The fossiliferous unit consists of a ~1 m thick set of stacked decimeter-scale very coarse sandstone bodies with Fe/Mn pisolites. specimen into a predefined group meaning that fossils for which This unit's microconglomeratic channels display abundant cross- there is no modern analog will nonetheless be grouped so this bedding and climbing ripples and have high concentrations of mud may not be an appropriate method for all samples. clasts at the bottom of the individual channels. The unit is erosively To better understand dietary patterns, a DFA was performed on truncated at the top and overlain by 1.5 m of red, locally fractured, a combined dataset including the first principal component (PC1) medium-grained sandstone (Fig. 2D). scores, which correlate with diet and capture overall occlusal The types of facies recognized in the AMD-45 outcrop and their shape, SQ, and M1 length, a proxy for body size. Among primates spatial orientation, all indicate that sedimentation took place in a there is a strong correlation between diet and body size with pri- fluvial environment, with frequent channelization in the coarse mates weighing less than 500e700 g largely consuming diets of sandstones and large over-bank deposits in the form of siltstones, insects, gum, or other high calorie food items (Kay, 1975; Kay and that were subsequently bioturbated. The fossil elements, con- Covert, 1984). Small-bodied insect-consuming primates and sisting of teeth, jaws, and bone fragments, are enriched in the large-bodied folivorous primates may have similar dental mor- coarse fraction. Sandstones and conglomerates are often cemen- phologies adapted to processing structural carbohydrate. The in- ted with dolomitic carbonates, as identified by XDIF analyses, clusion of a body size metric is important in an analysis where other indicating that the deposits have experienced some degree of functional variables (i.e., SQ and PC1) do not include body size in- burial and diagenesis that either replaced the original calcium formation. Extant species were grouped according their primary carbonate cement or provided the conditions for primary dolo- dietary components (frugivore, folivore, hard-object feeder, mitic cementation by tectonically induced fluid flow events. insectivore-frugivore, and exudate specialist) based on dietary in- Various outflows of hydrothermally heated waters along the formation compiled from Allen and Kay (2012), updated with present-day Río Alto Madre de Dios support the latter mechanism recent literature. Extinct species were left ungrouped. All analyses for dolomite mineralization. Other postdepositional deformation were conducted in SPSS v. 24 (IBM Corp., 2016). Results were cross- includes extensional faulting, mostly accommodated in the validated using ‘leave one out classification’ and prior probabilities structurally weaker siltstones, likely caused by the extensive were set to equal. The efficacy of the model was determined by folding during the formation of the Salvacion Syncline- correct classification rates. Pantiacolla Anticline complex. R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 5

Figure 2. Geographic location and Cenozoic stratigraphy of the Río Alto Madre de Dios region, Peru. A) Map of Peru showing the geographic position of the village of Atalaya. B) View of the AMD-45 locality from the top of the outcrop. C) Geologic basemap of the Salvacion Syncline and Río Alto Madre de Dios area showing the contacts between the named formations; redrawn after Vílchez and Romero (1998). D) Stratigraphic profile of AMD-45 site. Fossils, including the primate, come from the conglomerate at the 18e19 m level. Symbols for panel C: yellow filled circles ¼ biostratigraphic age (Ma) from Louterbach (2014); red-filled circles ¼ detrital zircon maximum depositional age (Ma); green-filled circles ¼ apatite fission track ages (Ma) from Keenan (2008) and Louterbach (2014). Fission track ages given with standard error. Radiometric ages for AMD localities are based upon samples reported in this paper and in Salenbien (2018). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

3.3. Radiometric age determinations measured to be ~10 m thick; a second sample is situated in the coarse sandstone at the base of AMD 45 exposure, 15 m below Three detrital zircon samples constrain the depositional age of the fossil-bearing layer. A third detrital sample was obtained AMD-45. The ﬁrst sample (AMD-63) is situated stratigraphically from locality AMD-57 which is ~500 m stratigraphically above 10 m below the base of the measured AMD-45 section in Figure 2 the AMD-45 locality and represents the youngest mapped lo- and is separated from the AMD-45 section by a large conglom- cality of the Bala Formation on the western ﬂank of the Salvacion erate outcrop that prevented continuous mapping but is Syncline. 6 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

Detrital sample AMD-63 has a maximum depositional age of Formation and age Bala Formation, between 18.9 ± 0.7 Ma and 18.9 ± 0.7 Ma at 1s based on the youngest grain out of 407 retained 17.1 ± 0.7 Ma. ages, providing an upper age constraint for the AMD-45 locality, as Diagnosis In having a hypocone situated on a strong distolingual the age of the youngest detrital zircon grain dictates the oldest cingulum the new species resembles most Oligocene to Early possible sedimentary age of the host sediment. The maximum Miocene platyrrhine taxa with which it can be compared (Brani- depositional age for the AMD-57 is determined to be 17.1 ± 0.7 Ma, sella Hoffstetter, 1969, Canaanimico Marivaux et al., 2016a, Maz- based on the youngest grain out of 116 retained ages (YSG age). This zonicebus Kay, 2010, Chilecebus Flynn et al., 1995, Panamacebus youngest age constrains a lower age for the fossil locality and co- Bloch et al., 2016, Tremacebus Hershkovitz, 1974, Dolichocebus incides with the youngest age for the hosting Bala Formation Kraglievich,1951, Soriacebus Fleagle et al.,1987, Carlocebus Fleagle, (Roddaz et al., 2010; Salenbien, 2018). Sample AMD-45 did not yield 1990,andHomunculus Ameghino, 1891). In its small size, the zircon grains of such young age, but the two youngest detrital ages hypocone is similar to that in Branisella and Canaanimico. Perupi- are 21.9 ± 0.5 and 22.6 ± 0.5 Ma out of 440 retained ages, and are thecus Bond et al., 2015 has a very small cristiform hypocone. outside the 1s range of the AMD-63 YSG age. Combining the detrital Presence of a hypocone is a distinction from extant callitrichine U/Pb dates, a radiometrically-derived maximum age bracket can be platyrrhines, which have strong cingula but lack hypocones or set at between 17.1 ± 0.7 and 18.9 ± 0.7 Ma for the AMD-45 locality. have very small ones, as in Callimico Ribeiro,1912. Parvimico differs Two other pieces of data support the proposed age based on our from all the above Miocene taxa in its small size, suggesting an U-Pb dates. 1) Apatite ﬁssion track (AFT) dates were previously animal similar to extant Callithrix Erxleben, 1777 and Mico Lesson, reported from the eastern ﬂank of the Salvacion Syncline (Kennan, 1840, among the smallest of living platyrrhines (less than 250 g). A 2008; see our Fig. 2C). Two of these AFT dates fall in a similar distinguishing combination of features that set Parvimico apart stratigraphic position to the above-reported U-Pb dates and have from the above penecontemporaneous Patagonian platyrrhines ages of 18.7 ± 3.99 Ma and 18.7 ± 2.82 Ma. 2) Marivaux et al. (2012) includes the presence of a well-developed stylar shelf adorned proposed a biostratigraphic age based on a nearby small-mammal with a cristiform mesostyle, the absence of paraconule and met- fauna as pre-Santacrucian, i.e., ‘Pinturan’, an Argentine faunal age aconule and their crests, a short and distally oriented post- ranging 18.75e16.5 Ma (Fleagle et al., 2012; Perkins et al., 2012).4 protocrista, absence of a prehypocrista and hypometacrista, Combining the age information provided by the U-Pb dates of the weakly developed hypoparacrista, and an overall dental pattern detrital zircon, the previously reported AFT ages, and the that is characterized by low crests and acute cusps. biostratigraphic age constraints derived from the same geological formation, it is unlikely that the AMD-45 is older than 18.9 ± 0.7 Ma or younger than 17.1 ± 0.7. 4.1. Description

IPVF-5000 is a complete and virtually unworn left M1. The roots 4. Systematic paleontology are not preserved and there are no interstitial facets mesially or distally, suggesting a tooth that was in the process of eruption but Class Mammalia Linnaeus, 1758 not yet in full occlusion. The metacone and paracone are slightly Order Primates Linnaeus, 1758 damaged postmortem but the tooth is otherwise intact. Suborder Anthropoidea Mivart, 1864 The mesiodistal length of the tooth is 2.12 mm and the bucco- Infraorder Platyrrhini Geoffroy Saint-Hilaire, 1812 lingual breadth is 2.84 mm, as measured on the virtual recon- Family incertae sedis struction. The nearly equal size of paracone and metacone and the Parvimico gen. nov. large size of the stylar shelf buccal to the metacone make it more likely that the tooth is an M1 and not an M2. Based on the area of the LSID zoobank.org:act:B339ED2Ce8B88-4FA7-AE68-0E07FE8F tooth in comparison with M1 size in other platyrrhines, we estimate B299. that this species was smaller than 250 g (see subsection 5.1). Type species Parvimico materdei gen. et sp. nov. With compensation for postmortem damage, the paracone is Etymology From Latin ‘parvus’ (tiny) and ‘mico’ (monkey in slightly larger and more projecting than the metacone, and the Spanish and Portuguese). preparacrista and postmetacrista are symmetric. The metacone and Diagnosis As for the type and only known species. paracone are widely separate leaving the postparacrista and premetacrista much longer than the preparacrista and postmetacrista. All four buccal crests are aligned mesiodistally. The preparacrista Parvimico materdei sp. nov. and postmetacrista both are supported by moderately-sized para- (Fig. 3) style and metastyle. The stylar cusps grade buccally into a raised stylar shelf. The latter supports several enamel swellings along its LSID zoobank.org:act:0159DF55-67A2-4C82-A33D-4AFE491E2 length among which is a cristiform mesostyle that is free-standing 6B7. and not attached to the premetacrista or postmetactista. Etymology In reference to the Río Alto Madre de Dios on the banks Paraconule and metaconule and their respective crests are ab- of which the fossil was found. sent. A rounded and poorly deﬁned anterior transverse crista Holotype IPVF-5000 (ﬁeld code AMD-45-01), a left M1 (Figs. 3 and (hypoparacrista) arises from the paracone and leads lingually into 4) housed at the Instituto de Paleontología, coleccion de Ver- the trigon but is unattached to any crest or cusp at its lingual end. A tebrados Fosiles, Universidad Nacional de Piura, Piura, Peru. hypometacrista is absent. Type locality AMD-45 left bank of the river, ~11 km below Atalaya, The protocone is tranverse to, and slightly distal to the paracone Madre de Dios Province, Peru. Coordinates: 12.8059 S; rather than being more distal to the paracone, as in most calli- 71.394 W. trichines. The strong preprotocrista arises from the protocone and reaches along the buccal margin of the crown to reach the parastyle. The postprotocrista runs distobuccally a short distance before 4 The ‘Pinturan’ age is early Santacrucian. The age range and contained faunas of the Pinturas Formation is generally older than that of the coastal Santa Cruz For- curving more buccally towards the base of the metacone. In a highly mation but overlaps it in western exposures (Kramarz and Bellosi, 2005). unusual morphology (not seen in any other platyrrhine), only the R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 7

Figure 3. Left M1 of Parvimico materdei gen. et sp. nov. (IPVF-5000, holotype) from the Early Miocene (Santacrucian SALMA) of Alto Madre de Dios locality AMD-45, Peruvian Amazonia: A) stereopair in occlusal view; B) mesial view; C) lingual view; D) distal view. E) buccal view. proximal segment of the postprotocrista is salient whereas its distal smaller than any previously known fossil platyrrhine (Table 2). A part becomes indistinct well before it reaches the base of the met- bivariate plot of M1 mesiodistal length plotted against acone. The postprotocrista lacks a distal spur directed towards the buccolingual breadth (Fig. 5) indicates that Parvimico molar hypocone (e.g., it lacks a crest that is sometimes analogized with the dimensions are on the lower end of the range for Saguinus ‘Nannopithex fold’ of early euprimates). The hypocone is small and is labiatus and Callithrix argentata, but is distinctly larger than distal and lingual to the protocone. A prehypocrista is absent leaving Cebuella pygmaea, the smallest platyrrhine monkey. Parvimico is protocone and hypocone separated by a deep sulcus. also distinctly smaller than the recently described Perupithecus A well-developed lingual cingulum runs from the apex of the (471e523 g; Bond et al., 2015), from the Late Eocene or Early hypocone lingually around the base of the protocone delineating a Oligocene Santa Rosa locality, which falls within the upper range wide cingulum shelf, although it does not reach to the pre- for our S. labiatus specimens. protocrista mesially. The lingual cingulum is unadorned by a peri- Shearing quotients Table 3 summarizes the molar shearing and cone or other cusps. A raised posthypocrista runs distobuccally and mesiodistal lengths by genus for small bodied platyrrhines grades into a raised distal marginal cingulum, before terminating in (Saimiri and extant callitrichines). The full dataset for individual a small mesostyle. specimens is reported in SOM Table S2. The formula derived from 1 In combination, small body size, the presence of a small hypocone, the PGLS model is ‘Expected’ upper ﬁrst molar shear ¼ M length the absence of molar conules and their associated crests, faintly visible * 0.92507 þ 0.23585. For the PGLS regression we found a strong 2 hypoparacrista, absent hypometacrista, strong buccal and lingual phylogenetic signal: Pagels l equals 1.0000. The multiple R value 2 cingula, and reduced importance of a postprotocrista render the for this relationship is 0.996, while the adjusted R ¼ 0.995. By morphology of the upper molar of Parvimico distinct from that of any comparison with the upper molars of other extant platyrrhines known living or fossil platyrrhine species. Nevertheless, while in (data from Allen et al., 2015), extant callitrichines all have Parvimico we identiﬁed no unique synapomorphies with any living moderately developed shearing crests, falling among frugivores family of platyrrhines, it has many similarities of uncertain polarity and hard object feeders but outside the range of shearing typical with many different and unrelated extant and extinct platyrrhine taxa. for larger bodied-folivores (Fig. 6A). When subdivided based on percentage of fruit, exudate, and insect consumption, the following trends appear: 5. Results Saguinus and Callimico, who consume more insects (and also 5.1. Paleobiology fungi for Callimico, which contains considerable structural carbohydrate) than other callitrichines (Porter, 2001), have well- Body size Body mass estimates reconstructed from Egi et al.'s developed shearing crests (higher SQ). (2004) anthropoid and total sample equations produced body Callithrix, a frugivore with a high consumption of exudates, has sizes of 239 and 232 g, respectively, indicating that Parvimico is only moderately-developed M1 shearing crests. 8 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

Figure 5. Bivariate plot of M1 buccolingual breadth (in mm) against mesiodistal length for species of small-bodied platyrrhines: the callitrichines Leontopithecus rosalia, Saguinus fuscicollis nigrifrons, Callithrix penicillata and Cebuella pygmaea, and the cebine Saimiri boliviensis. The molar dimensions of Parvimico materdei are on the lower end of the range for S. fuscicollis and C. penicillata, but distinctly larger than Ce. pygmaea, the smallest living platyrrhine monkey. The dimensions of Perupithecus ucalayensis are considerably larger. Data from living species from Plavcan (1990).

Figure 6B illustrates M1 shearing quotients (SQ) for smaller- bodied platyrrhines (callitrichines and Saimiri) binned into six diet categories. Compared to extant platyrrhines, Parvimico falls well within the frugivore range (moderate shearing) and on the intermediate to lower end of the range for more insect consuming Figure 4. Dental nomenclature used in this study labeled on an occlusal view of the platyrrhines (higher shearing). Parvimico does not, however, over- left M1. of Parvimico materdei gen. et sp. nov. (IPVF-5000, holotype). Terminology lap with any of the exudate consuming callitrichines in our sample. follows Kay (1977) with modiﬁcations (Marivaux, 2006). Landmark analysis The PCA results of the GPA-aligned landmark Cebuella pygmaea, whose diet consists primarily of exudates, has points of the M1 of the sample are summarized in Tables 4 and 5. the least developed molar shearing of any callitrichine. PC1 (24.5% of variance) is largely driven by the relationship between Leontopithecus, predominantly frugivorous, has moderately cusp tip landmarks (landmarks 1, 2, 4) and the landmark identifying developed shearing overlapping with all diet categories. It is the lowest point in the trigon basin (landmark 10; data matrix and important to note, however, that only two specimens of Leonto- factor loadings in SOM S3). Species with more negative PC1 values pithecus were accessible for this study and the inclusion of addi- have M1 with lower cusp relief (e.g., Pithecia, Chiropotes, Cacajao, tional specimens would likely expand this range signiﬁcantly. Cebus), while individuals in more positive PC1 space have molars

Table 2 Estimated body size of ?Early Oligocene to Early Miocene platyrrhines from M1 area.a

Taxon Geologic age Mean M1 area Number of Egi et al. (2004) anthropoid Egi et al. (2004) total sample equation specimens equation

Perupithecus ucayalensis Early Oligocene 9.10 1 497 477 Branisella boliviana Late Oligocene (Deseadan) 12.73 1 899 848 Carlocebus carmenensis Early Miocene 30.17 3 3548 3207 (Colhuehuapian) Chilecebus carrascoensis Early Miocene 14.31 1 1106 1036 (Colhuehuapian) Dolichocebus Early Miocene 21.88 1 2342 2144 gaimanensis (Colhuehuapian) Parvimico materdei Early Miocene (Santacrucian) 6.02 1 239 235 Mazzonicebus almendrae Early Miocene 21.42 3 2367 2077 (Colhuehuapian) Panamacebus transitus Early Miocene 26.25 1 3231 2928 (Colhuehuapian) Soriacebus ameghinorum Early Miocene 19.12 3 1856 1711 (Colhuehuapian) Homunculus patagonicus Early Miocene (Santacrucian) 23.37 1 2385 2182 Lagonimico conclucatus Middle Miocene (Laventan) 15.75 1 1310 1221 Stirtonia victoriae Middle Miocene (Laventan) 60.90 1 14292 12380 Stirtonia tatacoensis Middle Miocene (Laventan) 47.08 1 9070 7966 Cebupithecia sarmientoi Middle Miocene (Laventan) 17.77 1 1621 1501 Neosaimiri ﬁeldsi Middle Miocene (Laventan) 13.50 9 988 937

a Body mass was calculated in two ways: 1) From the anthropoid equation of Egi et al. (2004):lnBM¼ 1.767 * ln (M1 area) 4.555 (RE ¼ 0.950); and 2) from the total primate sample of Egi et al. (2004):lnBM¼ 1.713 * ln (M1 area) 4.535 (RE ¼ 1.012). Ratio estimator (RE) is the correction for logarithmic transformation bias (Smith, 1993). R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 9

Table 3 Upper molar shearing measurements for smaller-bodied platyrrhines (under 1 kg) and Parvimico materdei gen. et sp. nov.

Genus n Diet M1 shear M1 length ln M1 shear ln M1 length Source

Callimico goeldii 8 Fruits, insects and fungi 3.65 2.85 1.29 1.05 This paper Callithrix argentataa 5 Fruits and exudates 2.90 2.42 1.07 0.88 This paper Cebuella pygmaeaa 4 Exudates 2.21 1.79 0.79 0.58 This paper Leontopithecus rosaliaa 2 Fruits 3.91 3.12 1.36 1.14 This paper Saguinus labiatus and Saguinus oedipus 6 Fruits, insects and exudates 2.96 2.45 1.09 0.90 This paper Saimiri boliviensis 9 Fruits and insects 3.66 2.75 1.30 1.01 Allen et al. (2012) Parvimico materdei 1 2.85 2.22 1.05 0.80 This paper

a Species included in the PGLS reference line. with taller cusps and lower basins (e.g., the callitrichines, Saimiri, protocone falling in a nearly direct buccolingual line with the par- Alouatta, Brachyteles; Fig. 7). This variation accords well with the acone towards the mesial aspect of the tooth. Individuals with more diet of the species and is a similar measure to SQ (e.g., taller cusps positive values along PC1 have a protocone positioned in a more will have longer shearing crests), though, information about shape distal position relative to the paracone. This is particularly apparent that may not be directly functional (e.g., position of the cusps in the callitrichine primates. relative to each other) is also incorporated. Individuals in more Along PC1, most of the fossil primates fall within the range of positive PC1 space tend to incorporate more structural extant primates that consume insects and leaves (e.g., Saimiri, carbohydrates (plant fiber or chitin) into their diet, while those in Alouatta) or are mixed feeders (e.g., Callicebus). Of particular note, negative PC1 space are, as a group, hard object consumers (e.g., Parvimico falls within the PC1 range of the callitrichines, Saimiri, Pitheciinae) or omnivores (e.g., Cebus). Frugivores fall between these Alouatta and Brachyteles, a position consistent with a diet that in- two groups in PC space and have a moderate degree of dental relief. cludes structural carbohydrates. Parvimico is far too small to have These include the atelines Ateles and Lagothrix. been a folivore, so the structural carbohydrate would have been In terms of overall shape of the occlusal surface, the pitheciines found in insect chitin. and Cebus (negative PC1 space) have quadrate molars with the Variation along the second principal component (PC2), ac- counting for 19.2% of the variance, is largely driven by the mesiodistal length of the tooth, with species falling along the more positive portion of the PC2 axis having teeth that are relatively wide buccolingually (e.g., the callitrichines). There appears to be little structuring by diet along this axis. All of the fossils fall within the range of extant platyrrhines along PC2 except for Xenothrix, which has a particularly mesiodistally long tooth. Combined analyses A DFA of SQ, PC scores, and molar length was used to classify extinct primate by diet (Table 6). The model was well-supported and Wilks’ lambda is statistically significant (p < 0.001). The results here were consistent with results reported above obtained from SQ. There was an overall 85.0% correct classification rate (percentages are cross-validated results) with classification errors most commonly occurring among frugivorous (77.4% correct classification) and exudate consuming primates (80.0% correct classification). Folivores were correctly classified 100% of the time, and hard object consumers 92.6% of the time, and primates consuming a mixed diet of fruit and insects had a correct classification rate of 82.4% (Table 6). Parvimico materdei was classified in the DFA as a consumer of insects and fruit, with a squared Mahalanobis distance (D2) to the centroid of insect/fruit eaters (1.74) that indicates that it falls relatively close to the centroid (the mean point of all variables in multivariate space) of the distribution of insect/fruit consuming primates. The mean of Mahalanobis distances to the centroid for insect/fruit consuming primates is 2.05 and the range is 0.45e7.06. Other fossil platyrrhines included in this analysis that were classified by diet with some degree of confidence include Neo- saimiri fieldsi (insect/fruit consumer; D range ¼ 1.1e1.9), two specimens of Carlocebus carmenensis (frugivore; D range ¼ 0.66e1.68), one specimen of Homunculus patagonicus (frugivore; D ¼ 0.93), and Soriacebus ameghinorum (frugivore; D ¼ 2.05). The Caribbean platyrrhines Antillothrix bernensis, Insu- Figure 6. Box-and-whisker plots of upper first molar shearing quotients (SQ) for all lacebus toussaintiana, and Paralouatta varonai, as well as Pan- extant platyrrhine genera binned by diet. A) SQs for extant platyrrhine genera and amanian Panamacebus transitus were classified as folivores; Parvimico binned into five categories. Data points represent species mean SQs. B) Only however, they all had D values well outside of the range observed platyrrhines with body masses less than 1 kg (the callitrichines: Leontopithecus rosalia, Saguinus fuscicollis, Callithrix penicillata, Cebuella pygmaea, and the cebine Saimiri for extant folivores, indicating that this classification may be sus- boliviensis) were plotted with dietary categories binned by percent fruit, exudate, and pect. Xenothrix mcgregori, was classified as a hard object consumer, insect intake (see Table 3). Data points represent individual SQs. but also fell at the edge of the distribution. 10 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

Table 4 Principal component analysis of generalized Procrustes analysis-aligned landmark points of the upper ﬁrst molars of extant and extinct platyrrhine taxa, as enumerated in Table 1.

PC1 (% variance) R2 and % of variance explained by centroid size PC2 (% explained variance) R2 and % of variance explained by centroid size

24.5% 0.009 and 0.95% 19.2% 0.31 and 31.36%

Abbreviations: PC ¼ principal component.

5.2. Phylogenetics contrast, a phyletic link between the tropics and Patagonia is found in Peruvian Late Oligocene Canaanimico, which links The results of the phylogenetic analysis are depicted in Figure 8. with Patagonian stem soriacebines Soriacebus and Mazzoni- Our analysis yields four equally parsimonious trees of 115,306 cebus confirming the assessment of Marivaux et al. (2016a). steps, with a CI of 0.304, a RI of 0.499 and a RC of 0.151. Five salient (3) The analysis supports the hypothesis of multiple overwater points emerge from the analysis: dispersal events of primates to the Greater Antilles (Hedges, 1996; Woods et al., 2018), as opposed to an Oligocene land (1) Parvimico falls outside the platyrrhine clade. It is positioned bridge connection between the Greater Antilles and South as the nearest sister taxon to crown anthropoids, closer to America (Iturralde-Vinent and MacPhee, 1999; MacPhee and crown Anthropoidea than to two North African Late Eocene Iturralde-Vinent, 2005). There appear to have been at least taxa, Proteopithecus and Catopithecus. As discussed below, two independent dispersals. Ancient DNA establishes that the placement of Parvimico may arise from the extremely Xenothrix and Callicebus (Cheracebus) are sister taxa that split poor record of this new taxondjust a single upper molar. at ~11 Ma (Woods et al., 2018). Cuban Paralouatta marianae is And, the branch length separating Parvimico from the of Early Miocene age, most probably between 18.5 and catarrhine platyrrhine node is extremely shortdParvimico is 17.5 Ma (MacPhee et al., 2003). So Paralouatta was present in very close to a morphology that would be expected for the the Greater Antilles independently and at a much earlier date LCA of the two. than Xenothrix. In our analysis Paralouatta is recovered as a (2) Most known platyrrhine taxa older than late Early Miocene stem platyrrhine sister to Hispaniolan Antillothrix. are stem platyrrhines (i. e., are outside the clade of the living (4) Two Early Miocene genera are evidently members of the platyrrhine families and their last common ancestor). Among Cebidae. Central American Panamacebus from 21 Ma falls the tropical taxa, Late Eocene/Early Oligocene Perupithecus is within the Cebinae clade, but varies in its position with an early offshoot of the platyrrhine clade, rather than linking respect to either Neosaimiri and Saimiri, or to Cebus. Simi- with a cluster of Late Eocene African taxa as proposed by larly, ~21 Ma Chilecebus from northern Chile links with Bond et al. (2015) and supported by the analysis of Marivaux cebines plus Aotus. Hitherto, comprehensive phylogenetic et al., 2016a. Late Oligocene Branisella is the second branch analyses had supported a stem platyrrhine position for from the stem platyrrhines. Several Early Miocene taxa from Chilecebus (Flynn et al., 1995; Kay, 2015b; Marivaux et al., Patagonia (Dolichocebus þ Tremacebus and 2016a). The difference arises from our scoring of added Homunculus þ Carlocebus) are independent stem lineages dental characters from the type skull of Chilecebus. The unrelated to any known tropical stem platyrrhine. In finding of cebid affinities of Chilecebus further supports an Early Miocene antiquity of Cebidae advocated by Bloch et al. (2016),confirming (and narrowing) dos Reis et al.‘s(2018) molecular clock estimate of the split between Cebidae and Table 5 Atelidae as occurring between 20 and 23.4 Ma. It follows Factor loadings for principal component analysis of generalized Procrustes analysis-aligned landmark points of the upper first that Atelidae and Pitheciidae must also have existed in the molars of extant and extinct platyrrhine taxa. Early Miocene, although we have no record of either until about 16 Ma, with the appearance of the pitheciin Proter- Landmark (in 3D) PC1 PC2 opithecia (Kay et al., 1998). X1 0.077 0.270 (5) Consistent with molecular clock studies that suggest an Early Y 1 0.176 0.072 Z1 0.448 0.176 Miocene date of divergence of the crown platyrrhine fam- X 2 0.421 0.167 ilies, Middle Miocene (Laventan South American land Y 2 0.235 0.172 mammal age [SALMA]; ~15.6 to 13 Ma) platyrrhines from Z 2 0.103 0.294 Colombia all cluster with various living platyrrhine families: X3 0.315 0.215 Lagonimico, Mohanamico, Neosaimiri are cebids; Stirtonia is Y 3 0.308 0.187 5 Z 3 0.144 0.112 an atelid, and Nuciruptor and Cebupithecia are pitheciids. X 4 0.115 0.029 Y4 0.035 0.061 6. Discussion and conclusions Z 4 0.116 0.264 X5 0.072 0.226 Y5 0.161 0.150 Parvimico is the first named Early Miocene primate from the Z 5 0.095 0.606 Amazon basin (an unnamed primate astragalus of similar age was X6 0.061 0.120 the first published record). The presence of primates from this time Y 6 0.081 0.082 interval is scarcely surprising given their previous record from Z 6 0.073 0.164 X7 0.133 0.178 older rocks at many localities in Peru, Bolivia, Chile, and Argentina, Y7 0.301 0.084 as well as the Greater Antilles and Central America. Nevertheless, it Z7 0.079 0.046 X 8 0.122 0.177 Y8 0.303 0.134 5 Patasola and Miocallicebus were not included in the analysis; the former is a Z8 0.004 0.006 cebid and the latter a pitheciid. R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 11

Figure 7. Plot of the two ﬁrst principal components (PC) resulting from a PCA of upper molar landmark data excluding the hypocone.

Table 6 Cross-validation results of a discriminant function analysis of upper first molar shearing quotient, first principal component, and natural logarithm of first molar length of living platyrrhine genera. Numbers in bold show the count and percentages of the specimens that were correctly classified.

Folivore Frugivore Hard object consumer Frugivore/insectivore Exudate consumer Total

Classiﬁcation count Folivore 20 00 0 020 Frugivore 1 41 34453 Hard object consumer 0 2 25 0027 Frugivore/insectivore 0 0 0 14 317 Exudate consumer 0 0 0 2 8 10 Percentage classiﬁcations Folivore 100.0 0.0 0.0 0.0 0.0 100.0 Frugivore 1.9 77.4 5.7 7.5 7.5 100.0 Hard object consumer 0.0 7.4 92.6 0.0 0.0 100.0 Frugivore/insectivore 0.0 0.0 0.0 82.4 17.6 100.0 Exudate consumer 0.0 0.0 0.0 20.0 80.0 100.0

provides a glimpse of a previously undocumented diversity, for 17.1 ± 2.4 Ma from a site that contains Miocene mammals, see example the early presence of marmoset- and tamarin-sized below (Antoine et al., 2013; see our Fig. 2). As with AMD-45, the platyrrhines. ages come from detrital zircons and not from primary ash-fall tuffs; thus, they only establish a maximum age for the sediments. 6.1. Geology and age Nevertheless, these dates are consistent with a Burdigalian (late Early Miocene) age. In terms of the scheme of SALMA, the equiva- ‘ ’ ‘ Radiometric dating On the basis of detrital U/Pb dates from detrital lent in Argentina would be early or pre-Santacrucian (the Pin- ’ zircons, the age of AMD-45 is bracketed between 18.9 ± 0.7 and turan fauna, see Kramarz and Bellosi, 2005). 17.1 ± 0.7 Ma. Biostratigraphic age Two other small Miocene-aged and one Two other age determinations are reported from the Bala For- Paleocene-aged faunas have previously been described in the Alto mation from apatite ﬁssion-tracks: 18.7 ± 3.99 (Kennan, 2008) and Madre de Dios region. Of primary interest is the complete right 12 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628

Figure 8. Four equally parsimonious trees recovered from a maximum parsimony analysis of living and fossil platyrrhines, selected African Eocene-Oligocene anthropoids, and representative extant catarrhines. The crown anthropoid clades are highlighted in color as follows: purple ¼ Catarrhini; green ¼ Pitheciidae; blue ¼ Atelidae; salmon ¼ Cebidae. The four phylogenies differ in the placement of Panamacebus within the Cebidae and the positioning of fossil pitheciins Nuciruptor, Cebupithecia, and Proteropithecia. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 13 astragalus of a platyrrhine described by Marivaux et al. (2012) from by Flynn et al. (1995; see also Kay, 2015a), but in agreement with locality MD-61, which roughly coincides with locality AMD-51 views expressed by Rosenberger et al. (2009). mapped during our fieldwork. The MD-61 locality is located The phylogenetic analysis places Parvimico outside the platyr- upstream of AMD-45, in close proximity to the port town of rhine clade and places it as a stem anthropoid closer to the last Atalaya, and belongs to the Bala Formation. Marivaux et al. (2012) common ancestor of platyrrhines and catarrhines than either the did not report radiometric age constraints for their fossil find, but North African Late Eocene anthropoid taxa Catopithecus or Proteo- instead provided biostratigraphical age constraints based on the pithecus. Such a finding is unlikely to be sustained as more material occurrence of Scleromys quadrangulatus, a small dinomyid becomes available. This placement outside the platyrrhine clade caviomorph rodent, or close ally of that taxon. This caviomorph is arises from the overall simplicity of Parvimico's molar pattern, with associated with the pre-Santacrucian ‘Pinturan’ association, absence of conules and strengthened buccal cingula, both of which ranging from 18.75 to 16.5 Ma (Kramarz and Bellosi, 2005; also are characteristic of the above-mentioned North African Late Kramarz, 2006; Kramarz et al., 2010), indicating a late Early Eocene taxa but uncommon in known platyrrhines. It may be that Miocene age. This makes MD-61 roughly concurrent with the the anatomy of the upper molars is of limited utility, used alone, to AMD-45 fossil locality described here. reconstruct platyrrhine phylogeny. The anatomy of the lower teeth, A second Miocene vertebrate fossil locality, MD-67, roughly particularly of the premolars, should resolve this question. For 19 km north and downstream of AMD-45, was reported by Antoine example, North African taxa of early anthropoids all have two- et al. (2013). As already noted, an apatite fission track age of rooted third and fourth lower premolars, whereas all living and 17.4 ± 2.4 Ma was given for this locality. Antoine et al. (2013) re- extinct platyrrhines have single-rooted lower premolars. If it were ported that the fossil site was washed away by the summer of 2011 shown that Parvimico had single-rooted lower premolars, its posi- and we were also unable to locate it in 2015 and 2016. The MD-67 tion would shift to the platyrrhine clade. fauna includes the marsupials Sipalocyon sp. and Marmosa Other anatomical evidence runs counter to the phylogenetic (Micoureus) cf. laventica. Sipalocyon has known temporal range of placement of Parvimico with African taxa. For example, Parvimico Colhuehuapian-Santacrucian (~21e16 Ma; Marshall,1981). Mar- has a better developed hypocone than the African stem anthro- mosa (Micoureus) laventica is Laventan (~13.5e12 Ma; Marshall, poids (parapithecids excepted), which have only a slight hypocone 1976). The rodent Guiomys sp. spans the Colloncuran (~15.5 Ma) development, or none at all. and Laventan (Vucetich et al., 2015); ‘Scleromys’ spp (Dinomyidae) A similar absence of information about the anatomy of Perupi- range from the Pinturan (19e17 Ma) through Laventan (Vucetich thecus, likewise known only from a single complete upper molar et al., 2015); cf. Microsteiromys sp. is Laventan (Vucetich et al., (and one half of another)6 led Bond et al. (2015) and Marivaux et al. 2015). Antoine et al. (2013) assigned this fauna to the Middle (2016a) to place this taxon among African anthropoids. The analysis Miocene, equivalent of the Laventan SALMA, based on the more presented here supports the placement of Perupithecus at the base derived marsupial and rodent material, with holdovers from the of the platyrrhine clade, not with African anthropoids. Early Miocene Colhuehuapian (~21 Ma), Pinturan, and Santacrucian (17e16 Ma). It is important to note, however, that the MD-67 fauna 6.3. Behavior is extremely fragmentary (only a few teeth) and the specimens are referred to species that come from between 1000 and 4500 km Parvimico was an exceptionally small monkey, in the size range away. Moreover, the fission track dates do not clarify the age of the of marmosets and tamarins (Callitrichinae). Despite its small size fauna beyond an Early or Middle Miocene range. there is no evidence for dwarfing or gum-eating as observed in A third fossil-yielding locality was reported by Louterbach et al. marmosets and tamarins (Ford, 1980; Rosenberger, 1984; Martin, (2014), consisting of a series of closely-spaced outcrops (MD-85, 1992). Dwarfing undoubtedly occurred in the callitrichine clade, MD-177, MD-184, MD-255) that have yielded a variety of vertebrate as it is nested within the Cebidae, all of which are larger-bodied. and invertebrate fossil material. Charophytes recovered from the Among other morphological peculiarities of callitrichines is a outcrops along with tooth material of fishes indicate a Paleocene reduction in the size of the molars, with the second molar greatly (Thanetian) age (59.2e56 Ma) and is corroborated by a recently reduced and the third molar often, but not always, absent; and reported U-Pb dating of detrital zircons with an age of 58.96 þ 3.0/- molar hypocones are small or absent throughout the molar row 3.8 Ma (Salenbien, 2018). Vertebrate material reported by (Kay, 1994). With Parvimico, we have a callitrichine-sized species Louterbach et al. (2014) did not include any mammal or unam- but with a small but discrete cingulum hypocone. That the hypo- biguously continental/freshwater vertebrates. cone was reduced on M2 of Parvimico seems unlikelyda clear sign Depositional environment All sites examined from the Bala For- of hypocone reduction would be a corresponding reduction in the mation along the Rio Alto madre de Dios, spanning the interval size of the metacone on the upper first molar, whereas the meta- between 30.3 and 17.1 Ma indicate that a fluvial depositional cone is similar in size to the paracone (Kay, 1994). regime without estuarine/marine influence (Salenbien, 2018). We considered what the structure of the upper first molar can tell us about the probable diet of Parvimico. Based on SQ alone, compared to extant platyrrhines, Parvimico's SQ falls within the 6.2. Phylogeny frugivore range (moderate shearing) and on the intermediate to lower end of the range for more insect-consuming platyrrhines Our overall phylogenetic scheme for extinct platyrrhines is (higher shearing). Parvimico does not overlap with any of the similar to that of Kay (2015b), as modified by Marivaux et al. exudate-consuming callitrichines in our sample. The landmark (2016a). The most significant modification is a change to the mo- analysis largely supports a reconstruction of a mixed fruit and in- lecular scaffold based on molecular phylogenetic study of Woods et sect diet. Parvimico falls within the PC1 range of the callitrichine al. (2018) that places Xenothrix as sister to some but not all Calli- and Saimiri, consistent with a diet that includes structural cebus. Some differences are notable, however. With addition of hitherto unscored upper dental characters, our analysis suggests placement of Chilecebus within the Cebidae, and therefore place- 6 A lower molar was figured by Bond et al. (2015) as a primate. However, several ment within the crown platyrrhine clade, and not a stem platyr- features of this specimen, especially the structure of the tooth roots, support an rhine. This result is a departure from the view previously expressed alternative allocation to a marsupial. 14 R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 carbohydrates. In the combined DFA of tooth size, SQ and PC1, faunadone for Paralouatta (and perhaps the Hispaniolan taxa) Parvimico was classified as a consumer of both insects and fruit, but and a second, later arriving ancestor of Xenothrix. not gum, as in extant marmosets. Entry into Central America The discovery of the cebid Pan- amacebus from the Early Miocene of Panama (Bloch et al., 2016) 6.4. Revised biogeographic scenario establishes that crown primates made a beachhead in Central America far earlier than assumed previously. Nevertheless, Kay (2015a, 2015b) presented a biogeographic scenario of the Panamacebus did not give rise to any extant Central American major features that contributed to platyrrhine evolution, taxon in situ. Instead, molecular phylogenetic analysis indicates combining phylogenetic evidence with the climatic and geologic that ancestors of modern Central American platyrrhines did not record. Discoveries since 2015 are generally consistent with Kay's reach Central America until the Pliocene (Lynch Alfaro, 2017). (2015a, 2015b) scenario, although a few more notable discoveries Regional extirpation Miocene extratropical platyrrhines living in are necessary and a revised phylogenetic analysis requires several Patagonia, Central America, and the Greater Antilles went extinct refinements. without leaving any living descendants. Patagonian and Central Rafting from Africa and early diversification Platyrrhines reached American taxa disappear at the end of the Early Miocene; those South America from Africa via rafting possibly as early as 41 Ma, from the Antilles remained as residents until approximately when caviomorph rodents of African origin first appear in the 4e1.5 Ma (Rímoli, 1977; Cooke et al., 2017). neotropics (Antoine et al., 2012). Over the next 15 million years, platyrrhine diversification was restricted to tropical South America with Parvimico appearing to be a part of this basal Acknowledgements radiation. Although its phylogenetic position is uncertain, unlike small-bodied callithrichines, which have lost or greatly reduced This work was supported by National Science Foundation the hypocone, Parvimico combines very small body size and (grants EAR 1338694 to P. A. B and R. F. K. and DDIG 0726134 to S. B. strong development of a hypocone, indicating that these two C.) and the National Geographic Society (Young Explorers Grant characteristics were not linked in platyrrhine evolution. Another 9920-16 to W.S. and Waitt Grant W449-16 to R.F.K.). We graciously important discovery was Perupithecus from the Early Oligocene thank the Instituto de Paleontología, Universidad Nacional de Piura, (31 Ma; Antoine et al., 2012). Our analysis suggests that this for hosting the expedition and housing all recovered AMD fossils fi Perupithecus is a stem platyrrhine rather than being more closely and continuing to pick screenwash matrix. The eld crew of ex- allied to North African Paleogene anthropoids, as proposed by peditions over 2016 and 2017 included Dorien de Vries (who found Bond et al. (2015) and Marivaux et al. (2016a). If so, then the primate), Miguel Ortega, Gustavo Bejar, Anthony Deza, David currently available evidence is consistent with one rafting event, Chavez, Alex Wheatley, Richard F. Kay, Lauren A. Gonzales, Wout ~ not two. (If Perupithecus is a stem catarrhine, not a stem Salenbien, Luis Angel Valdivia Covenas, Catherine Rigsby, and Paul platyrrhine as Bond et al., 2015 proposed, then two separate A. Baker. We especially thank the Machiguenga and Cusquenian rafting events would be required.) boatmen for their help navigating the Río Alto Madre de Dios and fi Intracontinental extratropical dispersal Several clades of platyr- its tributaries and their guidance in the eld. We are also indebted rhines dispersed from tropical South America to higher latitude to Marianne van Vlaardingen for assistance with travel and logis- localities in Patagonia at ~25e24 Ma via a ‘Parana Portal’ following tics. Laurent Marivaux, John Kappelman, Jonathan Bloch and David fi the regression of the Paranense Sea through eastern South America. Alba provided essential editing and valuable scienti c criticism. The timing of this dispersal event remains undisputed; the earliest occurrence of platyrrhines is still Colhuehuapian and none is found Supplementary Online Material in intensively sampled older Patagonian Deseadan. That several clades reached Patagonia independently is further supported by the Supplementary online material to this article can be found on- Late Oligocene presence in Peru of the stem clade Soriacebidae, line at https://doi.org/10.1016/j.jhevol.2019.05.016. otherwise known only in the Early Miocene of Patagonia (Marivaux fi et al., 2016a). A novel nding of our new analysis is that Chilecebus References may be a representative of the crown platyrrhine Cebidae, supporting Rosenberger's (1977, 1981) early views, not a stem Adams, D.C., Rohlf, F.J., Slice, D.E., 2004. Geometric morphometrics: Ten years of platyrrhine as Kay (2015a, 2015b) and others (Flynn et al., 1995; progress following the ‘revolution’. Italian Journal of Zoology 71, 5e16. Albert, J.S., Lovejoy, N.R., Crampton, W.G., 2006. Miocene tectonism and the sepa- Marivaux et al., 2016a) previously concluded. ration of cis-and trans-Andean river basins: Evidence from Neotropical fishes. Arrival in the Greater Antilles Kay (2015a, b) concluded that stem Journal of South American Earth Sciences 21, 14e27. platyrrhines dispersed by rafting from Northern South America to Allen, K.L., Kay, R.F., 2012. Dietary quality and encephalization in platyrrhine primates. Proceedings of the Royal Society B 279, 715e721. the Greater Antilles by the Early Miocene (Cuban Paralouatta at Allen, K.L., Cooke, S.B., Gonzales, L., Kay, R.F., 2015. Dietary inference from upper and 16e18 Ma; MacPhee et al., 2003) and not in the Early Oligocene lower molar morphology in platyrrhine primates. PLoS One 10, e0118732. (~34 Ma) via a proposed land bridge or island chain (GAARlandia; Ameghino, F., 1891. Nuevos restos de mamíferos fosiles descubiertos por Carlos Ameghino en el Eoceno inferior de la Patagonia austral: Especies nuevas, adi- Iturralde-Vinent and MacPhee, 1999). The hypothesis that many ciones y correcciones. Revista Argentina de Historia Natural 1, 289e328. Antillean platyrrhines are stem forms remains viable. But the Antoine, P.-O., Marivaux, L., Croft, D.A., Billet, G., Ganerød, M., Jaramillo, C., demonstration by Woods et al. (2018) using recovered molecular Martin, T., Orliac, M.J., Tejada, J., Altamirano, A.J., Duranthon, F., Fanjat, G., genetic data that Jamaican Xenothrix is a part of the ‘Callicebus’ Rousse, S., Gismondi, R.S., 2012. Middle Eocene rodents from Peruvian Ama- zonia reveal the pattern and timing of caviomorph origins and biogeography. clade has several profound implications for dispersal. Byrne et al. Proceedings of the Royal Society B 279, 1319e1326. (2018) recognized three genera formerly grouped as Callicebus, Antoine, P.-O., Roddaz, M., Brichau, S., Tejada-Lara, J., Salas-Gismondi, R., with a basal split occurring between Cheracebus and Altamirano, A., Louterbach, M., Lambs, L., Otto, T., Brusset, S., 2013. Middle þ Miocene vertebrates from the Amazonian Madre de Dios Subandean Zone, Callicebus Plecturocebus (~10 Ma). According to Woods et al. Perú. Journal of South American Earth Sciences 42, 91e102. (2018), Xenothrix is sister to Cheracebus. Therefore, Xenothrix is a Antoine, P.-O., Abello, M.A., Adnet, S., Altamirano Sierra, A.J., Baby, P., Billet, G., crown platyrrhine in the family Pitheciidae and must have Boivin, M., Calderon, Y., Candela, A., Chabain, J., Corfu, F., Croft, D.A., Ganerød, M., Jaramillo, C., Klaus, S., Marivaux, L., Navarrete, R.E., Orliac, M.J., arrived in Jamaica since 10 Ma. This points to a minimum of two Parra, F., Perez, M.E., Pujos, F., Rage, J.-C., Ravel, A., Robinet, C., Roddaz, M., separate rafting events to account for the Greater Antilles primate Tejada-Lara, J.V., Velez-Juarbe, J., Wesselingh, F.P., Salas-Gismondi, R., 2016. R.F. Kay et al. / Journal of Human Evolution 134 (2019) 102628 15

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