Journal of Human Evolution 59 (2010) 218e222 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol News and Views Stem taxa, homoplasy, long lineages, and the phylogenetic position of Dolichocebus Richard F. Kay a,*, John G. Fleagle b a Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA b Department of Anatomical Sciences, Health Sciences Center, Stony Brook University, Stony Brook, New York 11794-8081, USA article info identifying them as being members of a clade. In our analysis, a suite of derived anatomical features that are generally lacking in Article history: the Patagonian taxa unites all living, or crown, platyrrhines. Among Received 16 November 2009 other things, compared with the Patagonian taxa, crown platyr- Accepted 12 February 2010 rhines have a shorter rostrum, a more transversely arched palate, Keywords: more convergent orbits, reorganization of the arrangement of the Platyrrhini bones at pterion, larger, more transversely positioned premolar Phylogenetics metaconids, loss of molar hypoconulids and of a postentoconid Anthropoidea sulcus, and reduction of molar roots. It is the absence of the above- Molecular clocks listed derived features of crown platyrrhines in the Patagonian taxa that suggests each of them is a stem platyrrhine, and outside of the modern radiation. The Patagonian taxa may belong to a separate stem clade or they may be a paraphyletic group, one species of which may prove to be the sister to the most recent common In his reply to our recent paper (Kay et al., 2008) entitled “The ancestor of living platyrrhines. Either way, Dolichocebus, Trem- anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey acebus and the other less-well known Patagonian early Miocene from Argentina,” Rosenberger (2010: p.1) addresses a wide range of monkeys are stem platyrrhines. topics including the anatomy of the fossils, molecular dates for platyrrhine evolution, phylogenetic systematics, parallelism, and fl more broadly “the nature of phylogenetic, functional, and adaptive Re ections on homoplasy evidence in historical evolutionary reconstruction.” These are very large and complex topics, worthy of debate. Nevertheless, we will As Rosenberger notes, parallelism or homoplasy is present in all restrict our comments in this rebuttal to a few simple observations. evolutionary reconstructions of primate phylogeny. However, He “ Rosenberger rejects our conclusions that many of the fossil plat- (2010: p.4) chides us for failing to acknowledge that not all ” yrrhines from the early Miocene of Argentina are stem platyrrhines. homoplasy is created equal. While this may be true, most scholars, fi He (2010: p.1) claims that our “conclusion rests on a weakly sup- including us, agree that homoplasy can only be identi ed in the ’ ported cladistic artifact, a purported monophyletic group of context of a phylogenetic reconstruction. Rosenberger s reply southern platyrrhines.” Even more clearly, Rosenberger (2010: p.2) mirrors his 2002 essay (Rosenberger, 2002) emphasizing the states “A plethora of issues cast doubt on the reliability of Kay et al.’s problems posed by homoplasy for the type of phylogenetic analyses (2008) ‘stem group’ hypothesis.” He claims that the “central tenant” used in our paper. He repeats several widely perceived miscon- of our stem group hypothesis is that early Miocene Dolichocebus, ceptions about homoplasy as a phenomenon. One is that the pres- Tremacebus, Carlocebus, and Soriacebus form a clade. But our ence of homoplasy in an analysis is some sort of analytical artifact hypothesis does not rest on this ‘central tenant.’ Rosenberger is rather than an evolutionary reality. Another is that the presence of “ ” either misrepresenting our position or completely misunder- homoplasy is the result of using the wrong kinds of characters. A fl standing of the concept of stem taxa (see Williams and Kay, 1995; third is that the level of homoplasy in an analytical result re ects the fi Williams et al., 2010). con dence one can have in the resulting tree. All studies of homo- Contrary to what Rosenberger claims, our identification of the plasy in phylogeny reject these views (e.g., Sanderson and Patagonian fossils, including Dolichocebus, as stem platyrrhines Donoghue, 1989, 1996; Sanchez-Villagra and Williams, 1998; outside the clade of living platyrrhine genera is not dependent on Lockwood and Fleagle, 1999). It is often suggested that homoplasy is more common in some types of characters than others and therefore analyses using such * Corresponding author. characters are likely to generate high levels of homoplasy and E-mail address: [email protected] (R.F. Kay). unreliable results (e.g., Collard and Wood, 2000, 2001). Certainly it 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.03.002 R.F. Kay, J.G. Fleagle / Journal of Human Evolution 59 (2010) 218e222 219 is true that, in any given analysis, different types of characters may between Dolichocebus and Saimiri are not even observable because show different levels of homoplasy (e.g., Ross et al., 1998). However, the relevant areas are broken away in the fossil. In his reply, these seem to be idiosyncratic results from individual analyses of Rosenberger continues to dwell on the phylogenetic significance of particular taxa and cannot be generalized from one analysis or one the midsagittal profile of the frontal bone (glabellar region) and the group of taxa to another (Lockwood and Fleagle, 1999). All broad shape and size of its underlying frontal cortex and olfactory bulbs. comparative studies of homoplasy have found no evidence that any The midsagittal part of the frontal bone is not preserved in Doli- particular type of data (e.g., molecular, osteological, dental, chocebus. Rosenberger agrees, but states that Dolichocebus’ glabella behavioral) consistently shows higher levels of homoplasy than must have been ‘domed’ as it is in Saimiri and Cebus because the another (e.g., Sanchez-Villagra and Williams, 1998; Lockwood and natural endocast of the frontal lobe of the neocortex is expanded in Fleagle, 1999). There are no general rules. Thus, features that may Dolichocebus. Specifically, he (2010: p.3) claims that Dolichocebus is be extremely labile in one clade may be essentially fixed in another. similar to cebines (Saimiri and Cebus): “the prominent olfactory For example, fusion of the mandibular symphysis has occurred bulbs and high arc of the frontal lobedthe underlying morphology several times in strepsirrhines and perhaps only once in crown of import, as stateddare well preserved and clearly show the anthropoids. The entepicondylar foramen of the humerus was lost anterior braincase had a cebine-like, domed shape rather than the many times in platyrrhines but only a few times in catarrhines. flat frontal region which is primitive among NWM.” We find three While homoplasy unquestionably makes the reconstruction of problems with this argument. First, the profile of the frontal cortex phylogenetic relationships more difficult, and character evolution of Dolichocebus is not domed as it is in Cebus and Saimiri. Second, more “messy” than one might prefer, it is a real evolutionary the olfactory bulbs of the fossil differ markedly from those of Sai- phenomenon that is present at all levels of biological analysis from miri and Cebus. And third, comparison of this part of the braincase amino-acid sequences to aspects of adult bony morphology and in extant platyrrhines demonstrates that the glabellar region of the behavior. Certainly there are methodological ways of generating frontal cannot be inferred from the endocranial profile of the “spurious” homoplasy in an analysis (e.g., through aspects of char- frontal cortex. acter definition) and ways of artificially minimizing the amount of With respect to the first two points, Rosenberger correctly states homoplasy in a phylogenetic tree (e.g., by arbitrarily eliminating that Saimiri and Cebus both have a high arc to the frontal bone, the characters with high homoplasy levels in all trees). However, ‘domed’ condition. Undoubtedly this is a correlative of the enlarged homoplasy is not primarily a result of methodological mistakes, but neocortex in these two species compared to most other NW rather the result of a variety of well-established evolutionary monkeys (Stephan et al., 1981; Fig. 1). The enlarged cebine frontal phenomena, including the nature of the genetic code, functional and neocortex expands dorsally over the olfactory fossae leaving the developmental constraints, allometry, and especially parallel or fossae ventral to the frontal lobes, not projecting rostral to it (Fig. 1A convergent adaptation (Lockwood and Fleagle, 1999). and D). In contrast, in Callicebus, the frontal lobes are smaller, and While recognizing the existence of homoplasy, Rosenberger the midsagittal profile of the frontal lobes is sloping, not ‘domed’ takes the view that certain character complexes are unlikely to (Fig. 1C and F). The olfactory bulbs of Callicebus are no larger than appear in parallel in New World monkeys (NWM) because they those of cebines (bulb volume data from Baron et al. [1983]), but reflect a fundamental niche partitioning that was entrained very they project rostrally in front of the frontal lobes. However, early in platyrrhine evolution and, once set in motion, has contrary to Rosenberger’s claims, Dolichocebus more closely continued to the present day. In his view it is to those characters resembles Callicebus than cebines: the midsagittal profile of its that we should turn a priori in placing extinct platyrrhines into frontal endocast is sloping and the olfactory fossae of Dolichocebus a phylogeny. However, as noted above, most reviews of homoplasy projects far rostral to the neocortex (Fig. 1E). In short, in having indicate that “reliable” characters are only evident after an analysis a sloping frontal neocortex and rostrally projecting olfactory fossae, and cannot be identified in advance. Dolichocebus displays the primitive platyrrhine condition, like Beyond the theoretical issues raised by Rosenberger’s paper Callicebus, not the derived Saimiri-Cebus morphology.