Elsevier

Journal of Human Evolution

Volume 122, September 2018, Pages 1-22
Journal of Human Evolution

Oldest evidence for grooming claws in euprimates

https://doi.org/10.1016/j.jhevol.2018.03.010Get rights and content

Abstract

Euprimates are unusual among mammals in having fingers and toes with flat nails. While it seems clear that the ancestral stock from which euprimates evolved had claw-bearing digits, the available fossil record has not yet contributed a detailed understanding of the transition from claws to nails. This study helps clarify the evolutionary history of the second pedal digit with fossils representing the distal phalanx of digit two (dpII), and has broader implications for other digits. Among extant primates, the keratinized structure on the pedal dpII widely varies in form. Extant strepsirrhines and tarsiers have narrow, distally tapering, dorsally inclined nails (termed a ‘grooming claws’ for their use in autogrooming), while extant anthropoids have more typical nails that are wider and lack distal tapering or dorsal inclination. At least two fossil primate species thought to be stem members of the Strepsirrhini appear to have had grooming claws, yet reconstructions of the ancestral euprimate condition based on direct evidence from the fossil record are ambiguous due to inadequate fossil evidence for the earliest haplorhines. Seven recently discovered, isolated distal phalanges from four early Eocene localities in Wyoming (USA) closely resemble those of the pedal dpII in extant prosimians. On the basis of faunal associations, size, and morphology, these specimens are recognized as the grooming phalanges of five genera of haplorhine primates, including one of the oldest known euprimates (∼56 Ma), Teilhardina brandti. Both the phylogenetic distribution and antiquity of primate grooming phalanges now strongly suggest that ancestral euprimates had grooming claws, that these structures were modified from a primitive claw rather than a flat nail, and that the evolutionary loss of ‘grooming claws’ represents an apomorphy for crown anthropoids.

Introduction

Most extant primates have fleshy-tipped fingers and toes with flattened nails (ungulae) instead of sharp claws (falculae). Indeed, the presence of ungulae is often hypothesized to characterize the common ancestor of extant primates, possibly associated with the evolution of manual dexterity (Jones, 1916, Napier, 1961, Le Gros Clark, 1971, Cartmill, 1974, Soligo and Müller, 1999, Soligo and Martin, 2006, Bloch et al., 2007). Exceptions to the ubiquity of these traits include the presence of tegulae (a falcula-like morphology) found in the aye-aye (Daubentonia madagascariensis) and in marmosets and tamarins (Callitrichidae). However, it is likely that tegulae secondarily evolved from the flattened ungulae more typical among primates (Hamrick, 1998, Soligo and Müller, 1999). Another exception to the ubiquity of ungulae in extant primates is the form of the keratinized structure supported by the distal phalanx of the second digit (dpII) of the foot. In some primates the pedal dpII resembles a dorsally projecting falcula more than a flattened ungula and is referred to as a ‘grooming claw,’ or ‘toilet claw,’ to reflect its observed use in autogrooming and/or scratching (Fig. 1). Groups exhibiting such a ‘grooming claw’ include strepsirrhines (lemurs, lorises, and galagos) and at least the owl monkey (Aotus) and titi monkey (Callicebus) among New World monkeys. In addition, tarsiers have a similar ‘grooming claw’ on both the second and third pedal digits (Soligo and Müller, 1999, Maiolino et al., 2011, Maiolino et al., 2012, von Koenigswald et al., 2012, Maiolino, 2015).

Studies such as those by Maiolino et al. (2011) have shown that ungulae, falculae, tegulae and ‘grooming claws’ have underlying distal phalanges with distinctive, correlative morphology. Thus, it is possible to infer which type of keratinized structure was present in extinct primates based on fossilized distal phalanges. Primarily, ungular phalanges are distinguished by dorsoventral flattening, mediolateral expansion, and a distally shifted attachment for the long flexor tendon. Falcular phalanges and tegular phalanges tend to be dorsoventrally expanded, mediolaterally narrow and to have a shaft that is plantarly curved and hook-like (Patel and Maiolino, 2016). In addition, ungular and ‘grooming claw’ phalanges of primates tend to have an ‘apical tuft,’ a fan- or apron-like sheet of bone that rims the distal tip (Maiolino et al., 2011, Maiolino et al., 2012).

Debates about the appropriate terminology for the ‘grooming claw’ stem from different perspectives on (1) the morphological features that distinguish ‘grooming claw’-bearing distal phalanges (grooming phalanges) from the bony phalanges underlying more typical falculae (falcular phalanges) and ungulae (ungular phalanges), and (2) the homology of these structures (Maiolino et al., 2011, von Koenigswald et al., 2012, Gebo et al., 2015).

Understanding the functional, developmental and phylogenetic basis of ‘grooming claw’ morphology contributes to understanding the evolutionary pattern of morphological divergence of euprimates from other euarchontans. More complete understanding of ‘grooming claw’ taxonomic distribution and morphological variation helps constrain hypotheses on the number of times these different morphologies arose and the selective pressures experienced by early primates. Below we briefly review previous perspectives on ‘grooming claw’ taxonomic distribution and homology to provide context and highlight the broader implications of the fossils described here.

It has been suggested that ‘grooming claws’ of ‘prosimians’ were inherited from the last common ancestor of modern primates (Soligo and Müller, 1999, Franzen et al., 2009), and that the lack of ‘grooming claws’ in extant anthropoids is likely an apomorphy. The presence of a ‘grooming claw’ in extant Aotus has been used as evidence against the latter point (Maiolino et al., 2011). Eocene adapiforms (possible stem strepsirrhines) have consistently been found to possess ‘grooming claws’. Fossil species previously known to have grooming claws include Notharctus tenebrosus (Maiolino et al., 2012), Europolemur koenigswaldi (von Koenigswald et al., 2012), Hoanghonius stehlini (Gebo et al., 2015), and Adapoides troglodytes (Gebo et al., 2017).

Even as the above cited evidence of ‘grooming claws’ in early fossil species was accumulating, Maiolino, von Koenigswald, Gebo and their collaborators interpreted the data and observations to indicate multiple independent evolutionary origins for the ‘grooming claw’ within euprimates. Maiolino et al. (2012) suggested that the mosaic morphology of the Notharctus ‘grooming claw’ (AMNH FM 143612-3) could indicate that it was in the process of evolving a ‘grooming claw’ from a more primitive condition that lacked ‘grooming claws’. Assuming adapiforms do indeed represent stem strepsirrhines, this would suggest convergence in ‘grooming claw’ morphology between at least strepsirrhines and haplorhines. Similarly, von Koenigswald et al. (2012) asserted that ‘grooming claws’ evolved independently in primates at least three times (once in strepsirrhines, once in tarsiers, and once in the ancestor of Aotus and Callicebus). Ni et al. (2013) reported additional evidence consistent with the view of convergent acquisition of ‘grooming claws.’ They described the foot of the basal haplorhine, Archicebus achilles, and interpreted the pedal dpII as lacking a grooming claw. By implying that ‘grooming claw’ traits evolved multiple times in different lineages from an ungula, these studies question the appropriateness of the term ‘grooming claw’.

While the lack of a ‘grooming claw’ in A. achilles would seem to be strong evidence against the homology of ‘grooming claws’ in strepsirrhines and haplorhines, there are problems with the evidence from this specimen. Primarily, the evidence amounts to an impression of the dpII in dorsal view. Maiolino et al., 2011, Maiolino et al., 2012 have demonstrated that a dorsal view alone is insufficient for diagnosing the presence of a ‘grooming claw’ in extant species known to have one.

Therefore, resolution of the form of the pedal dpII in the ancestral euprimate requires additional data from other early primate taxa, particularly from omomyiform primates—the radiation of Paleogene primates considered more closely related to extant haplorhines, and particularly tarsiids (Beard et al., 1988, Seiffert et al., 2009, Gingerich, 2012). In this context, if omomyiforms were found to exhibit an ungula-like structure on the pedal dpII (i.e., to lack a grooming claw), this would add convincing support to the hypothesis that ‘grooming claws’ evolved convergently in strepsirrhines and haplorhines. To date, omomyiform distal phalanges have been too sparsely represented to evaluate the form of the pedal dpII.

While it is impossible to unequivocally establish the lack of a ‘grooming claw’ in a fossil taxon without articulated material, the diagnostic features of grooming claws do make it possible to demonstrate their presence even from isolated remains. In this study, we describe seven distal phalanges (Table 1) that indicate the presence of ‘grooming claws’ in omomyiform primates. These fossils come from three different time intervals in the early Eocene of Wyoming, USA: (1) Bighorn Basin screen-washing sites in Wa0 (Wasatchian North American Land Mammal Age, Wa0 biozone) exposures of Willwood Formation (Fig. 2A) where Teilhardina brandti dentitions and postcrania are known to occur (Rose et al., 2011); (2) Washakie Basin screen-washing sites in Wa3 to Wa5 exposures of the Wasatch Formation (Fig. 2B), from whence a diversity of omomyiform dentitions have been recovered (Savage and Waters, 1978, Williams and Covert, 1994, Cuozzo, 2002); and (3) the Omomys Quarry site from the Bridger Basin (Fig. 2C), which is Br3 (Bridger North American Land Mammal Age, Br3 biozone) in age (Anemone and Covert, 2000, Murphey et al., 2001, Murphey et al., 2017). Three dimensional (3D) scans of the specimens are deposited and available for download and analysis on MorphoSource.org (Boyer et al., 2016), and can be directly accessed through the unique media identifiers and digital object identifier (DOI) links given in Table 1.

Sorting through screen-wash concentrate from Wa0 localities in the southern Bighorn Basin, P.E.M. and J.I.B. identified three distal phalanges with strong qualitative affinities to the grooming phalanges of extant primates (UF 334000, UF 409804, and UF 411197). The Wa0 biozone has only two species attributed to euprimates: a small omomyiform (T. brandti) and a much larger adapiform (Cantius torresi). The small size of the Wa0 distal phalanges immediately suggested that of these two euprimate candidates, the omomyiform is the most likely. In some regards, these fossil grooming phalanges appear more primitive than the grooming phalanges of extant primates, primarily in retaining a large basal nutrient foramen (Fig. 3).

These fossils were collected as part of an ongoing effort led by crews from the University of Florida and Duke University to increase representation of small vertebrate fossils from sites bracketing and sampling the Paleocene-Eocene Thermal Maximum (PETM) in the Bighorn Basin of Wyoming (Wing et al., 2005, Chester et al., 2010, Secord et al., 2012, Baczynski et al., 2013, Bourque et al., 2015).

Sorting through screen-wash concentrate from Wa3 and Wa5 localities of the Washakie Basin, D.M.B. recovered an additional three specimens (UCMP 217999, 218000, 218344) that appear qualitatively to resemble grooming phalanges of extant primates (Figure 2, Figure 3). Generally speaking, primates are extremely abundant from these sites: D.M.B. recovered 27 ungular phalanges (Fig. 2B; Supplementary Online Material [SOM] Table S1) and a total of 395 postcranial specimens attributable to omomyiforms based on their small size and comparisons to previously identified postcranial material of omomyiforms (Szalay, 1976, Savage and Waters, 1978, Dagosto, 1988, Gebo, 1988, Covert and Hamrick, 1993, Dagosto et al., 1999, Hamrick, 1999, Anemone and Covert, 2000, Dunn et al., 2006, Gebo et al., 2012), adapids (Gregory, 1920, Hamrick and Alexander, 1996), and extant primates.

An attribution to omomyiforms again seems most likely for the three grooming phalanges. An attribution to adapiforms seems unlikely given the small size of the bones, the low abundance of adapiform fossils at the sites, and apparent morphological differences between the new fossils and previously described adapiform dpII's (Maiolino et al., 2012, von Koenigswald et al., 2012, Gebo et al., 2015). On the other hand, the Washakie Basin grooming phalanges look quite similar to the Bighorn Basin grooming phalanges (including the presence of a large nutrient foramen; Fig. 2).

Interestingly, the Washakie Basin phalanx sample includes specimens from differently aged sites: UCMP 217999 (from UCMP locality V70214) and UCMP 218344 (from V7132) are older (Wa3), while UCMP 218000 (V74022) is younger (Wa5). UCMP 217999 and 218000 are essentially the same size, but likely represent different taxa since no large omomyiform species spans the Wa3-5 interval at these localities. UCMP 218344 is substantially smaller, suggesting the presence of a ‘grooming claw’ in a third omomyiform taxon. There are a minimum of two omomyiform taxa at each of the screen-washing sites yielding grooming phalanges (Table 2, Table 3).

The Washakie Basin fossils were collected primarily by Don Savage, J. Howard Hutchison, and University of California crews in the 1970s (Savage and Waters, 1978). Fossils were preserved in extensive shell marls and/or fine grained mudstones topping these marls. Stratigraphically- and geographically-constrained quarries were developed in these fossiliferous horizons. Quarries were screen-washed in small batches (shovel scoops) and sorted over several decades at the University of California, Berkeley. Specimen associations have been maintained to the level of the ‘shovel scoop’ of matrix.

During fieldwork in June 2017, surface collecting around Omomys Quarry (UCM L93026) located in the Hickey Mountain Limestone, Twin Buttes Member of the Bridger Formation (Anemone and Covert, 2000, Murphey et al., 2001, Murphey et al., 2017), yielded a bone qualitatively resembling a grooming phalanx of a small primate (DPC 25505; Figure 2, Figure 3). Because of this discovery, one of us (S.A.M.) re-examined previously-collected specimens from Omomys Quarry held at the University of Colorado, but did not recover any additional grooming phalanges. The fieldwork is part of a project starting in 2014 wherein crews led by J.I.B. and D.M.B. have surface prospected and quarried classic sites in Bridger B, C, and D (NSF BCS-1440742, 1440588).

Section snippets

Institutional and collection abbreviations

AMNH: American Museum of Natural History, New York, USA; DPC: Duke Lemur Center, Division of Fossil Primates collection, Durham, NC, USA; ECA: the Quercy locality of Escamps, France; FLMNH: Florida Museum of Natural History, Gainesville, FL, USA; FM: Fossil Mammals division of AMNH collection; M: Mammalogy division of AMNH collection; SBU: Stony Brook University, Stony Brook, NY, USA; UCM: University of Colorado Museum of Natural History, Boulder, CO, USA; UCMP: University of California Museum

Results

The results are organized into several sections below. In the first section, we describe results of several different ways of comparing shapes among samples of distal phalanges. The second section evaluates which fossil species known from teeth at the sites yielding the grooming phalanges may be the owners of the grooming phalanges. The third section evaluates the phylogenetic significance of the results.

Taxonomic attribution

Three fossil distal phalanges from the Bighorn Basin (UF 409804, 334000, and 411197), another three from the Washakie Basin (UCMP 217999, 218000, and 218344), and one from the Bridger Basin (DPC 25505) are grooming phalanges assignable to omomyiforms based on: (1) their strong morphological similarity to the grooming phalanges of extant strepsirrhines and/or tarsiers, and (2) an absolute size that is proportionally correct for the omomyiform teeth and ungular phalanges from the sampled

Summary and conclusions

Newly described specimens and comparative analyses provide the first compelling evidence that members of the omomyiforms, one of the two early Eocene euprimate radiations, possessed ‘grooming claws’ on at least the second pedal digit. Second pedal digit grooming claws are now documented in all major extant euprimate groups except for catarrhines, and with the evidence provided by the fossil record, they appear to be ubiquitous in strepsirrhines and non-anthropoid haplorhines. This wide

Acknowledgements

We thank G.F. Gunnell and C. Riddle of the Duke Lemur Center Division of Fossil Primates, and N. Simmons, E. Westwig and N. Duncan of the American Museum of Natural History for approving and facilitating loans of comparative material. We thank J. Thostenson for scanning specimens. NSF grants to D.M.B. and E.R. Seiffert (BCS-1317525), to D.M.B. and G.F. Gunnell (BCS-1440742), to D.M.B., G.F. Gunnell and R.F. Kay (DBI-1458192), to J.I.B. (BCS-1440558), D.M.B. (BCS-1552848), S.A.M. (BCS 1341075),

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