City University of New York (CUNY) CUNY Academic Works Publications and Research Brooklyn College 2012 Evidence for a Grooming Claw in a North American Adapiform Primate: Implications for Anthropoid Origins Stephanie Maiolino Stony Brook University Doug M. Boyer CUNY Brooklyn College Jonathan I. Bloch University of Florida Christopher C. Gilbert CUNY Hunter College Joseph Groenke Stony Brook University How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/bc_pubs/76 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] Evidence for a Grooming Claw in a North American Adapiform Primate: Implications for Anthropoid Origins Stephanie Maiolino1*, Doug M. Boyer2*, Jonathan I. Bloch3, Christopher C. Gilbert4, Joseph Groenke5 1 Stony Brook University, Stony Brook, New York, United States of America, 2 Brooklyn College, City University of New York, Brooklyn, New York, United States of America, 3 Florida Museum of Natural History, University of Florida, Gainesville, Florida, United States of America, 4 Hunter College, City University of New York, New York, New York, United States of America, 5 Stony Brook University, Stony Brook, New York, United States of America Abstract Among fossil primates, the Eocene adapiforms have been suggested as the closest relatives of living anthropoids (monkeys, apes, and humans). Central to this argument is the form of the second pedal digit. Extant strepsirrhines and tarsiers possess a grooming claw on this digit, while most anthropoids have a nail. While controversial, the possible presence of a nail in certain European adapiforms has been considered evidence for anthropoid affinities. Skeletons preserved well enough to test this idea have been lacking for North American adapiforms. Here, we document and quantitatively analyze, for the first time, a dentally associated skeleton of Notharctus tenebrosus from the early Eocene of Wyoming that preserves the complete bones of digit II in semi-articulation. Utilizing twelve shape variables, we compare the distal phalanges of Notharctus tenebrosus to those of extant primates that bear nails (n = 21), tegulae (n = 4), and grooming claws (n = 10), and those of non-primates that bear claws (n = 7). Quantitative analyses demonstrate that Notharctus tenebrosus possessed a grooming claw with a surprisingly well-developed apical tuft on its second pedal digit. The presence of a wide apical tuft on the pedal digit II of Notharctus tenebrosus may reflect intermediate morphology between a typical grooming claw and a nail, which is consistent with the recent hypothesis that loss of a grooming claw occurred in a clade containing adapiforms (e.g. Darwinius masillae) and anthropoids. However, a cladistic analysis including newly documented morphologies and thorough representation of characters acknowledged to have states constituting strepsirrhine, haplorhine, and anthropoid synapomorphies groups Notharctus tenebrosus and Darwinius masillae with extant strepsirrhines rather than haplorhines suggesting that the form of pedal digit II reflects substantial homoplasy during the course of early primate evolution. Citation: Maiolino S, Boyer DM, Bloch JI, Gilbert CC, Groenke J (2012) Evidence for a Grooming Claw in a North American Adapiform Primate: Implications for Anthropoid Origins. PLoS ONE 7(1): e29135. doi:10.1371/journal.pone.0029135 Editor: Anjali Goswami, University College London, United Kingdom Received July 20, 2011; Accepted November 21, 2011; Published January 10, 2012 Copyright: ß 2012 Maiolino et al. 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. Funding: Brooklyn College, The City University of New York and a Professional Staff Congress - City University of New York (PSC-CUNY) grant to DMB (ENHC-42- 122 Award #64733-00 42) supported this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (DMB); [email protected] (SM) Introduction are sometimes distilled into other subfamilies), and another subfamily, the Asiadapinae, are usually grouped together in the The oldest fossil euprimates are known from the Late family Notharctidae. Additionally, two other groups of adapiforms Paleocene-Eocene of Africa and the Eocene of North America, are recognized, the European and Asian Adapinae and the late Europe, and Asia. There are two major radiations of early surviving Sivaladapinae from Asia. euprimates: the adapiforms and the omomyiforms. Adapiforms are The relationship of adapiforms to living primate groups has a highly diverse group variously classified in a number of always been a matter of debate. Recently, this debate has been re- subfamilies: Notharctinae, Cercamoniinae, Caenopithecinae, Dje- kindled by the discovery of an exceptionally complete skeleton of belemurinae, Asiadapinae, Adapinae, and Sivaladapinae. the European cercamoniine Darwinius masillae [6]. Disagreement Notharctines are known exclusively from North America and about the phylogenetic significance of its morphology highlights include for example Cantius, Notharctus, and Smilodectes. Cercamo- the need for more complete documentation of early euprimate niinae has traditionally referred to many genera from Europe, anatomy [7] as well as a more quantitatively rigorous and broadly North America, Asia, and Africa including Europolemur, Donrussellia, acceptable (by researchers with different philosophies on phylog- Cercamonius, Caenopithecus, Mahgarita, Djebelemur, Aframonius, and eny reconstruction) analytical framework [8]. Anchomomys among others [1]. However, more recent analyses have suggested the separation of some into their own subfamilies: Hypothesized relationships of adapiforms to extant Caenopithecus, Aframonius, and Mahgarita, along with Afradapis, are primate clades considered caenopithecines by some [2,3]. It has also been Two major hypothesized relationships between adapiforms and suggested that Djebelemur and ‘Anchomomys’ milleri are more closely extant primates have been suggested. One position is that related to strepsirrhine primates than other adapiform groups, and adapiforms share a special relationship with crown strepsirrhines as such, this clade is sometimes referred to as the djebelemurines as either a paraphyletic stem or monophyletic sister group e.g., [2,4,5]. Notharctines, cercamoniines (including those genera that [9,10,11,12,13,14]. Alternatively, other researchers have suggested PLoS ONE | www.plosone.org 1 January 2012 | Volume 7 | Issue 1 | e29135 Grooming Claw in Adapiform Primates that adapiforms are more closely related to crown anthropoids strepsirrhines [2] rather than haplorhines [6]. This result suggested e.g., [15,16,17,18,19,20,21,22,23,24,25]. that similarities shared between Darwinius (and other caenopithe- A great number of shared similarities have been cited to link cines, like Afradapis) and haplorhines could be interpreted as the adapiforms and extant strepsirrhines. However, many of these result of convergent evolution. Additionally, Williams et al. [7] similarities can be explained as plesiomorphic (primitive) primate noted that a short rostrum, symphyseal fusion, and a deep characteristics [1,26,27]. These include the presence of a mandible have evolved in multiple euprimate lineages (both postorbital bar, an unfused mandibular symphysis (in the oldest strepsirrhine and haplorhine), while vertical, spatulate incisors and most primitive species, e.g. Cantius and Donrussellia), a ring-like could be interpreted as primitive for euprimates. Complete ectotympanic within the petrosal bulla, a relatively long snout, and symphyseal fusion is also absent in early haplorhines, including a median gap between the upper central incisors associated with some early undisputed anthropoids from the Fayum [7,34]. wet-nose strepsirrhinism. However, several similarities in the Williams et al. [7] further argue that a vertically oriented postcranial morphology of adapiforms and strepsirrhines are talofibular facet might also be primitive for euprimates; they absent in other primates as well as other eutherian mammals; these interpret a vertical orientation in Darwinius as a secondary could be interpreted as shared-derived characteristics (synapo- reversion to this condition, while maintaining that its presence in morphies) linking the two groups. These include a talus with a haplorhines is a primitive retention. They also suggest that the gently sloping talofibular-joint facet, a groove for the tendon of M. polarity of the absence of a grooming claw is unclear, and suggest flexor hallucis longus that is positioned lateral to the posterior portion that a nail on the second pedal digit might be the primitive of the tibiotalar joint, and a large posterior trochlear shelf (though primate condition. this is reduced in some adapines and the caenopithecine Afradapis Building on these ideas, Gingerich et al. [8] performed a [26]); a navicular on which the articular facet for the cuboid is cladistic analysis using a matrix of 30 characters coded for fewer contiguous with both those for the ectocuneiform and the