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And the Taxonomy of the Yellow-Tailed Woolly Monkey, Lagothrix flavicauda

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And the Taxonomy of the Yellow-Tailed Woolly Monkey, Lagothrix flavicauda AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 137:245–255 (2008) Taxon Combinations, Parsimony Analysis (PAUP*), and the Taxonomy of the Yellow-Tailed Woolly Monkey, Lagothrix flavicauda Luke J. Matthews1* and Alfred L. Rosenberger2,3 1Department of Anthropology, New York University, New York Consortium in Evolutionary Primatology (NYCEP), New York, NY 10003 2Department of Anthropology and Archaeology, The Graduate Center, Brooklyn College, The City University of New York, Brooklyn, NY 11210 3Department of Mammalogy, The American Museum of Natural History, New York Consortium in Evolutionary Primatology (NYCEP), New York, NY 10024 KEY WORDS cladistics; taxonomy; taxon combinations; PAUP; parsimony; tree inference; New World monkeys; ateline systematics ABSTRACT The classifications of primates, in gen- results indicate that alternative selections of species sub- eral, and platyrrhine primates, in particular, have been sets from within genera produce various tree topologies. greatly revised subsequent to the rationale for taxonomic These results stand even after adjusting the character decisions shifting from one rooted in the biological spe- set and considering the potential role of interobserver cies concept to one rooted solely in phylogenetic affilia- disagreement. We conclude that specific taxon combina- tions. Given the phylogenetic justification provided for tions, in this case, generic or species pairings, of the pri- revised taxonomies, the scientific validity of taxonomic mary study group has a biasing effect in parsimony distinctions can be rightly judged by the robusticity of analysis, and that the cladistic rationale for resurrecting the phylogenetic results supporting them. In this study, the Oreonax generic distinction for the yellow-tailed we empirically investigated taxonomic-sampling effects woolly monkey (Lagothrix flavicauda) is based on an ar- on a cladogram previously inferred from craniodental tifact of idiosyncratic sampling within the study group data for the woolly monkeys (Lagothrix). We conducted below the genus level. Some recommendations to mini- the study primarily through much greater sampling of mize the problem, which is prevalent in all cladistic species-level taxa (OTUs) after improving some charac- analyses, are proposed. Am J Phys Anthropol 137:245– ter codings and under a variety of outgroup choices. The 255, 2008. VC 2008 Wiley-Liss, Inc. There have been significant shifts in the practice of analysis and interpretation of the alpha taxonomy of the primate systematics during the last decade. One involves New World woolly monkeys. From a taxonomic perspec- the use of parsimony algorithms (often implemented in tive, Groves’ (2001) book, Primate Taxonomy, is revolu- PAUP*) for reconstructing cladistic relationships. This tionary, reflecting all of the aforementioned types of re- approach has become ubiquitous. Another is the toler- vised taxonomic thinking, so his assessment deserves ance for highly split taxonomies (of the modern forms) close scrutiny. For the platyrrhine primates, for example, that have been put forth on the basis of limited study, he recognized 112 species. By comparison, two prior au- for example, naming newly discovered populations as thoritative classifications of the previous generation, by distinct species or even genera, elevating the rank of rec- Napier (1976) and Napier and Napier (1967), recognized ognized subspecies to the species level, reclassifying con- 64 and 67 species, respectively. geners into distinct genera, and multiplying the number Our main purpose is to increase awareness regarding of families within adaptive radiations (exemplary cases the effect of incomplete taxonomic sampling on phyloge- include Rylands et al., 2000; Groves, 2001). The ration- netic results for ateline primates presented in Groves ale for these taxonomic revisions is often the phyloge- (2001). Taxonomic sampling effects have been noted pre- netic position and distinctiveness of a taxon or taxa as viously in theoretical (Siddall, 1995; Graybeal, 1998; inferred by parsimony analysis of characters. The scien- tific justification for such cladistic taxonomic philosophy is well articulated in Cracraft (1983, 2002). This unitary Grant sponsor: Tow Faculty Travel Fellowship, Brooklyn College (City University of New York), and a PSC CUNY Research Award. justification—phylogenetics—departs from more tradi- tional taxonomic decisions, which have been based on *Correspondence to: Luke J. Matthews, Department of Anthropol- the biological species concept in the designation of spe- ogy, New York University, 25 Waverly Place, 4th Floor, New York, cies and on the balance between phylogeny and adapta- NY 10003. E-mail: [email protected] tion in the case of the genus and suprageneric taxa. Given this more restricted rationale, new taxonomies Received 20 August 2007; accepted 18 March 2008 pivot on the phylogenetic work that they represent, or the nonambiguous nature of the results. DOI 10.1002/ajpa.20859 In this work, we present a critique of one project that Published online 23 May 2008 in Wiley InterScience reflects the intersection of these trends, Groves’ (2001) (www.interscience.wiley.com). VC 2008 WILEY-LISS, INC. 246 L.J. MATTHEWS AND A.L. ROSENBERGER Hawks, 2004), genetic (Collins, 2001, 2003; Hillis et al., poeppigii). As an arbitrary matter of convenience, we fol- 2003), and morphological (Rosenberger and Kearney, low Groves’ usage. Previously, Rosenberger et al. (1996), 1995; Sargis, 2007; Silcox, 2007) studies, but we show tending to agree with C. Groves, in part, because of our they operate quite powerfully on the sort of morphologi- mutual familiarity with the specimens in the AMNH, also cal data coded in discrete character states that can be raised the rank of L. flavicauda. They proposed Oreonax scored relatively quickly from museum specimens and as a subgenus of Lagothrix. Others have also begun to that form the basis for important reassessments of pri- recognize Oreonax as a full genus (Rylands, 2000; mate taxonomy (e.g., Groves, 2001). We show that the Rylands et al., 2000) based on Groves’ work. Given the cladistic position obtained by Groves (2001) for the yel- narrow scope of this study, we use the nomina Oreonax low-tailed woolly monkey (Lagothrix flavicauda), which and L. flavicauda interchangeably. is the sole justification for the resurrection of the Groves’ judgment to raise the rank of L. flavicauda was generic nomen Oreonax, is likely an artifact of incom- based on a parsimony analysis of cranial characters using plete taxonomic sampling. The taxonomic-sampling PAUP 3.1.1 (Phylogenetic Analysis Under Parsimony; effects remain even after we corrected inaccurate delim- Swofford, 1993) to generate a hypothesis of cladistic itations of metric character states, controlled for the log- interrelationships among several ateline species. He per- ical interdependance of some characters, and ruled out formed two sets of studies. One focused on the four mod- interobserver reliability as an alternative cause of dis- ern ateline genera, Alouatta, Lagothrix, Ateles, and Bra- crepancies in tree topologies. At a more theoretical level, chyteles. Excluding L. flavicauda and L. lagotricha, the our study addresses a somewhat different point than species used in this analysis were not identified but were previous studies that focused on the importance of the ‘‘...picked at random from the AMNH collection,’’ accord- number of taxa sampled (Siddall, 1995; Graybeal, 1998; ing to Groves (2001, p 93). A second study added two sub- Hawks, 2004; Hillis et al., 2003) in that we assess how fossil species (Protopithecus and Caipora; see Hartwig the information content present in specific taxon combi- and Cartelle, 1996) to the data matrix. In both cases, he nations influences phylogenetic results, although Gray- found that the species L. flavicauda was more closely beal (1988) addresses this latter issue in the context of linked with Ateles than with Lagothrix lagotricha. Argu- ‘‘long branch attraction’’ in genetic studies. Further- ing that the full assemblage of woolly monkeys cannot, more, the results of our study have obvious methodologi- therefore, be shown to be monophyletic, Groves opted to cal relevance to the study of fossil primates, which are place the species L. flavicauda in a genus of its own. pseudorandomly sampled because of taphonomic con- straints, and for which algorithmic parsimony has become a preferred method of inferring relationships (e.g., Kay et al., 1997; Strait et al., 1997; Strait and MATERIALS AND METHODS Grine, 1999; Seiffert et al., 2005). We conclude by mak- Materials ing several suggestions on how to fix the problem, one of which is simply to sample more taxa when they are The samples forming the basis of this study are from available, preferably of forms that are confidently collections of the American Museum of Natural History known to be cladistically relevant. (AMNH), although we also examined the two adult and one juvenile L. flavicauda specimens in the British Mu- seum. Our samples represent all the modern ateline gen- era and perhaps one-third or more of their species diver- Historical background sity, as well as three pitheciines, which were included as out-groups for the parsimony analyses. For genus Lago- Fooden (1963) was the first to revise woolly monkey thrix, we used four of the recognized taxa, L. lagotricha, taxonomy during the modern era. He recognized two L. cana, L. lugens, and L. poeppigii. We used only adult species, L. lagotricha, generally known as the (common) skulls and
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