In his recent article “Primates in the Eocene”, Gingerich (2012) presented a broad review of Eocene primate radiations and their place in the primate evolutionary tree, with a particular focus on Adapoidea. While synthetic reviews of early primate evolution are always welcome additions to the literature, within his larger analysis Gingerich (2012) specifically discussed two issues that deserve special comment, the first relating to the evolution of grooming claws within Adapoidea and the second relating to his phylogenetic interpretation of Darwinius and Adapoidea within the order Primates, which was supposedly based on a modification of our own final matrix in Maiolino et al. (2012). Unfortunately, as we will demonstrate below, in both cases the interpretations of Gingerich (2012) are unlikely to be correct.
First, Gingerich (2012) characterises the morphology of Notharctus pedal distal phalanges as “ambiguous”. In fact, there is very little ambiguity involved. The analyses provided in Maiolino et al. (2012) demonstrate quite conclusively, both metrically and visually, that pedal distal phalanges bearing grooming claws are readily separated from other unguis forms (ungulae = nails, falculae = non-primate claws, and tegulae = claw-like ungues of callitrichins and aye-ayes) on the basis of facet-shaft angle (FSA), volar feature length (VFL), and other distinctive measures. Univariate and multivariate analyses including FSA and VFL clearly indicate that Notharctus tenebrosus possessed a grooming claw on pedal digit II (Maiolino et al. 2012). To illustrate this point further, a simple bivariate plot of FSA and VFL divided by total phalanx length (TPL) from 512 primate pedal distal phalanges shows the stark distinction between grooming claw and ungula-bearing distal phalanges (Fig. 1). Strepsirrhine and tarsier phalanges that bear grooming claws are well-separated from ungula- and tegula-bearing forms (Fig. 1, dotted line within convex hull surrounding all grooming claws).
On the basis of FSA and VFL/TPL, Fig. 1 indicates that Notharctus venticolis (UM 102287), Cantius nuniensis (UM 102193), and Notharctus tenebrosus (AMNH 143612_3 and AMNH 129382) bore grooming claws, confirming the results of Maiolino et al. (2012) for Notharctus tenebrosus and extending them to notharctid pedal morphology, more generally. We note that Gingerich (2012) provides no compelling evidence to the contrary, and the discriminant analyses mentioned by Gingerich (2012) (see also von Koenigswald et al. (2012)) exclude FSA, VFL, VFL/TPL, and other distinctive measures. Until our results are contradicted by a proper study including diagnostic features such as FSA, VFL, and VFL/TPL, the analyses in Maiolino et al. (2012) remain the most comprehensive performed thus far and strongly support our interpretation. Furthermore, given that multiple species of Europolemur also had grooming claws on pedal digit II (von Koenigswald 1979; von Koenigswald et al. 2012), it seems quite likely that most adapoids, including Darwinius, possessed grooming claws, an obvious similarity with living strepsirrhines. To definitively assess the presence or absence of a grooming claw in Darwinius moving forward, an undistorted lateral view of the pedal distal phalanges illustrating FSA and other features will be necessary.
Second, and most importantly, Gingerich’s cladistic interpretation of Darwinius masillae is demonstrably false and, as it is based on our own dataset, demands a strong response. In his paper, Gingerich (2012) stated that after modifying only one of the codings in our final data set (blood supply to the brain in Notharctus from “complex” to “promontory dominant”), he produced a most parsimonious phylogenetic tree with Notharctus and Darwinius reconstructed as stem haplorhines (see his fig. 6). This is, in fact, not true. If one takes the final 39 character matrix in Maiolino et al. (2012) and makes the change Gingerich (2012) advocates to the cranial blood supply character, the four most parsimonious phylogenetic trees produced are exactly the same as originally reported, with Notharctus and Darwinius unambiguously reconstructed as strepsirrhines (see Figs. 2 and 3; matrix provided in supporting online information).
Therefore, even using Gingerich’s own preferred codings, the most parsimonious interpretation of the data is that Notharctus and Darwinius are strepsirrhines, not haplorhines. We would also like to point out that ongoing research supports our original coding of “complex” for Notharctus cranial blood supply, as both the promontory and stapedial branches of the internal carotid can be enlarged in the specimens we have examined (Welch et al. 2014). Using our final data matrix, the only way one can produce a tree where Notharctus and Darwinius are reconstructed as stem haplorhines, as reported by Gingerich (2012), is to eliminate a number of characters from the analysis. In other words, the hypothesis that Notharctus and Darwinius are haplorhines is only tenable if one willingly excludes relevant anatomy and phylogenetic information.
More broadly, we would like to stress the importance of considering multiple fossil taxa and large numbers of morphological characters when assessing primate phylogenetic relationships. For the sake of argument, the phylogenetic analysis here and those in Maiolino et al. (2012) were intentionally restricted to a relatively small number of characters and only a few fossil taxa with fairly complete skulls and associated postcrania, as advocated by Gingerich et al. (2010) and Gingerich (2012). Although our results demonstrate that even an abbreviated morphological analysis and cursory examination of the fossil record leads one to consider a position within Strepsirrhini as the most likely phylogenetic hypothesis for Notharctus and Darwinius (see Figs. 2 and 3), this limited approach largely ignores the broader Eocene fossil record outside of Darwinius, Notharctus, and Catopithecus and effectively excludes large pieces of phylogenetic information. While Gingerich et al. (2010) and Gingerich (2012) argue against the inclusion of many fossil taxa and characters on the basis that they are typically too incomplete, the inclusion of fossil taxa has been empirically demonstrated to be crucial in phylogenetic analyses because fossil taxa extend taxon sampling (e.g. Gauthier et al. 1988; Donoghue et al. 1989; Huelsenbeck 1991; Wiens 1998; Strait and Grine 2004), provide unique morphologies that help to refine assessments of character transformation (e.g. Gatesy and O’Leary 2001; Springer et al. 2001; Gatesy et al. 2003), and increase overall phylogenetic accuracy (e.g. Gauthier et al. 1988; Wheeler 1992; Zwickl and Hillis 2002). In addition, multiple studies have demonstrated that increasing the number of characters in an analysis generally increases phylogenetic accuracy (e.g. Wiens 2003a; 2003b; 2006; Gilbert et al. 2009) and that missing data is not a serious problem as long as character sampling is sufficiently robust (Wiens 1998; 2003a; 2003b; 2006; Wiens and Morrill 2011; Pattinson et al. 2014). No serious modern phylogenetic analysis denies these facts, and to argue otherwise is philosophically unsound, flying in the face of the past 25 years of research (e.g. Gauthier et al. 1988; Donoghue et al. 1989; Huelsenbeck 1991; Wheeler 1992; Gatesy and O’Leary 2001; Springer et al. 2001; Zwickl and Hillis 2002; Gatesy et al. 2003; Wiens 1998; Wiens 2003a; Wiens 2003b; Wiens 2006; Gilbert et al. 2009; Wiens and Morrill 2011). Not surprisingly, more comprehensive and inclusive studies following rigorous cladistic methodology confirm our narrow results and strongly refute Gingerich’s (2012) hypothesis (e.g. Boyer et al. 2010; Seiffert et al. 2010; Williams et al. 2010; Pattinson et al. 2014). Again, the only way that one can reconstruct Darwinius as a haplorhine, even using Gingerich’s own preferred codings, is to effectively ignore relevant phylogenetic information by unjustifiably excluding a number of important characters and taxa because they are “incomplete”. To us, this seems a poor way to conduct a phylogenetic study, particularly if the overall goal is phylogenetic accuracy. Therefore, while we can never know the true phylogeny of any group of extinct taxa, a full consideration of all available evidence at this time strongly suggests that Notharctus and Darwinius (and adapoids more broadly) are strepsirrhines and, contra Gingerich (2012), the data in Maiolino et al. (2012) have never supported any other alternative hypothesis.
References
Boyer, D. M., Seiffert, E. R., & Simons, E. L. (2010). Astragalar morphology of Afradapis, a large adapiform primate from the earliest late Eocene of Egypt. American Journal of Physical Anthropology, 143, 383–402.
Donoghue, M. J., Doyle, J. A., Gauthier, J., Kluge, A. G., & Rowe, T. (1989). The importance of fossils in phylogeny reconstruction. Annual Review of Ecology, Evolution, and Systematics, 20, 431–460.
Gatesy, J., & O’Leary, M. A. (2001). Deciphering whale origins with molecules and fossils. Trends in Ecology & Evolution, 16, 562–570.
Gatesy, J., Amato, G., Norell, M., DeSalle, R., & Hayashi, C. (2003). Combined support for wholesale taxic atavism in Gavailine Crocodylians. Systematic Biology, 52, 403–422.
Gauthier, J., Kluge, A., & Rowe, T. (1988). Amniote phylogeny and the importance of fossils. Cladistics, 4, 105–209.
Gilbert, C. C., Frost, S. R., & Strait, D. S. (2009). Allometry, sexual dimorphism, and phylogeny: a cladistics analysis of extant African papionins using craniodental data. Journal of Human Evolution, 57, 298–320.
Gingerich, P. D. (2012). Primates in the Eocene. In: T. Lehmann, S.F.K. Schaal (eds) Messel and the terrestrial Eocene - Proceedings of the 22nd Senckenberg Conference. Palaeobiodiversity and Palaeoenvironments, 92, 649–663.
Gingerich, P. D., Franzen, J. L., Habersetzer, J., Hurum, J. H., & Smith, B. H. (2010). Darwinius masillae is a haplorhine—reply to Williams et al. (2010). Journal of Human Evolution, 59, 574–579.
Godinot, M. (1992). Early euprimate hands in evolutionary perspective. Journal of Human Evolution, 22, 267–283.
Huelsenbeck, J. P. (1991). When are fossils better than extant taxa in phylogenetic analysis? Systematic Zoology, 40, 458–469.
Koenigswald, W. von (1979). Ein Lemurenrest aus dem eozänen Ölschiefer der Grube Messel bei Darmstadt. Paläontologische Zeitschrift, 53, 63–76.
Koenigswald, W. von, Habersetzer, J., & Gingerich, P. D. (2012). Pedal distal phalanges of the Eocene adapoids Europolemur and Darwinius compared to phalanges of Notharctus and other primates. In: T. Lehmann, S.F.K. Schaal (eds) Messel and the terrestrial Eocene - Proceedings of the 22nd Senckenberg Conference. Palaeobiodiversity and Palaeoenvironments, 92, 539–565.
Maiolino, S., Boyer, D. M., & Rosenberger, A. (2011). Morphological correlates of the grooming claw in distal phalanges of platyrrhines and other primates: a preliminary study. Anatomical Record, 294, 1975–1990.
Maiolino, S., Boyer, D. M., Bloch, J. I., Gilbert, C. C., & Goenke, J. (2012). Evidence for a grooming claw in a North American adapiform primate: implications for anthropoid origins. PLoS ONE, 7, e29135. doi:10.1371/journal.pone.0029135.
Pattinson, D. J., Thompson, R. S., Piotrowski, A. K., & Asher, R. J. (2014). Phylogeny, paleontology, and primates: do incomplete fossils bias the tree of life? Systematic Biology. doi:10.1093/sysbio/syu077.
Seiffert, E. R., Perry, J. M. G., Simons, E. L., & Boyer, D. M. (2010). Convergent evolution of anthropoid-like adaptations in Eocene adapiform primates. Nature, 461, 1118–1121.
Springer, M. S., Teeling, E. C., Madsen, O., Stanhope, M. J., & de Jong, W. W. (2001). Integrated fossil and molecular data reconstruct bat echolocation. Proceedings of the National Academy of Sciences of the United States of America, 98, 6241–6246.
Strait, D. S., & Grine, F. E. (2004). Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. Journal of Human Evolution, 47, 399–452.
Welch, E. C., Boyer, D. M., Yapuncich, G. S., Gunnell, G. F., Seiffert, E. R., & Bloch, J. I. (2014). Re-evaluation of promontorial arterial dominance in fossil adapiforms. American Journal of Physical Anthropology, 153(S58), 270.
Wheeler, W. C. (1992). Extinction, sampling, and molecular phylogenetics. In M. J. Novacek & Q. D. Wheeler (Eds.), Extinction & Phylogeny (pp. 205–215). New York: Columbia Press.
Wiens, J. J. (1998). Does adding characters with missing data increase or decrease phylogenetic accuracy? Systematic Biology, 47, 625–640.
Wiens, J. J. (2003a). Incomplete taxa, incomplete characters, and phylogenetic accuracy: is there a missing data problem? Journal of Vertebrate Paleontology, 23, 297–310.
Wiens, J. J. (2003b). Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology, 52, 528–538.
Wiens, J. J. (2006). Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics, 39, 34–42.
Wiens, J. J., & Morrill, M. C. (2011). Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Systematic Biology, 60, 719–731.
Williams, B. A., Kay, R. F., Kirk, E. C., & Ross, C. F. (2010). Darwinius masillae is a strepsirrhine—a reply to Franzen et al. (2009). Journal of Human Evolution, 59, 567–573.
Zwickl, D. J., & Hillis, D. M. (2002). Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.
Acknowledgements
We would like to thank D. Boyer, S. Almécija, and B. Patel for microCT scans from which measurements used in this response were taken. We thank Eileen Westwig, Neil Duncan (Department of Mammalogy, American Museum of Natural History), and Terry Kensler (Laboratory for Primate Morphology and Genetics, Caribbean Primate Research Center) for access to collections. We also thank the following for access and assistance with microCT scanning: Stefan Judex, Clint Ruben (Stony Brook University Center for Biotechnology), Grant Dagliyan, Tautis Skorka, Anita Krishnan (Molecular Imaging Center, University of Southern California), Morgan Hill, and Henry Towbin (Microscopy and Imaging Facility, American Museum of Natural History). This material is based upon work supported by the National Science Foundation under Grant nos. BCS-1341075 (SAM), BCS-1317525 (DMB), BCS-1440472 (DMB), BCS 1440472 (DMB), BCS 1316947 (SA); The Leakey Foundation (SAM; BAP); American Association of Physical Anthropologists Professional Development Grants (DMB; SA); and the National Institutes of Health, Grant no. 8 P40 OD012217-25 (Caribbean Primate Research Center).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(NEX 8 kb)
Rights and permissions
About this article
Cite this article
Gilbert, C.C., Maiolino, S.A. Comment to “Primates in the Eocene” by Gingerich (2012). Palaeobio Palaeoenv 95, 237–241 (2015). https://doi.org/10.1007/s12549-015-0184-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12549-015-0184-1