The phylogeny of Cetartiodactyla: The importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies
Introduction
The mammalian superorder Cetartiodactyla (whales and even-toed ungulates) contains nearly 300 species including many of immense commercial importance (cow, pig, and sheep) and of conservation interest and aesthetic value (antelopes, deer, giraffe, dolphins, and whales) (MacDonald, 2006). Certain members of this superorder count among the best studied organisms on earth, whether speaking morphologically, behaviorally, physiologically or genetically. Understanding the interrelationships among cetartiodactyl species, therefore, is of obvious importance.
Much of the recent phylogenetic work has focused either on higher level questions such as the placement of Cetacea with respect to Artiodactyla, and the monophyly and relationships among Cetartiodactylan suborders and families (e.g., Gatesy et al., 1999, Nikaido et al., 1999, Lum et al., 2000, Matthee et al., 2001, Murphy et al., 2001, Naylor and Adams, 2001, Thewissen et al., 2001, Hassanin and Douzery, 2003, Arnason et al., 2004, Reyes et al., 2004, Gu et al., 2007, Wada et al., 2007, O’Leary and Gatesy, 2008), or on lower level questions of some smaller clades within the superorder (e.g., Pitra et al., 2004, Ropiquet and Hassanin, 2004, Ropiquet and Hassanin, 2005, Hassanin and Ropiquet, 2004, Willows-Munro et al., 2005, Gilbert et al., 2006, Guha et al., 2007). Hence, while a consensus seems to be emerging from a range of datasets (morphology, mitochondrial and nuclear DNA, SINEs) on many of the higher level relationships (for reviews see Price et al., 2005, Hernandez and Vrba, 2005, May-Collado and Agnarsson, 2006, O’Leary and Gatesy, 2008), understanding of species-level phylogenetics across the superorder is patchy.
Detailed species-level phylogenies are of paramount importance for comparative studies (Harvey and Pagel, 1991). In general, statistical power of comparative methods increases as taxon sampling approaches completion and as resolution increases (both adding to the number of possible sister-taxon comparisons). In addition, many methods in the toolkit of comparative biology perform best when branch length estimates are available (e.g., Felsenstein, 2004, Bollback, 2006).
To date, however, the most comprehensive primary-data-based phylogenetic study on cetartiodactylans included only 51 extant species (Gatesy et al., 2002; note that May-Collado and Agnarsson, 2006 and May-Collado et al., 2007 included 90 and 92 species, respectively, but focused on Cetacea and O’Leary and Gatesy, 2008 include 64 species but focus on extinct taxa). By combining multiple types of data for a strategically chosen set of taxa Gatesy et al. (2002) and O’Leary and Gatesy (2008) offered strong hypotheses of higher level relationships within Cetartiodactyla. However, lack of a more detailed phylogeny limits the types of questions that can be address using the comparative method. To remedy this Lalueza-Fox et al., 2002, Price et al., 2005, (see also Hernandez and Vrba, 2005) combined multiple phylogenetic studies, and non-quantitative taxonomies, to produce a complete phylogeny of Cetartiodactyla using a supertree approach (Bininda-Emonds and Bryant, 1998, Bininda-Emonds et al., 2002). While representing a significant advancement, the supertree has some shortcomings (for a general critique of supertree techniques see e.g. Gatesy et al., 2002). For example, large portions of the tree are simply reflecting taxonomy, rather than quantitatively addressing species interrelationships. Equally important for its use for comparative studies, the resolution of the supertree is relatively low (59.9%) and it does not provide estimates of branch lengths. A better resolved phylogeny with branch lengths, even though taxon-incomplete, may represent a more powerful tool for many comparative questions and methods.
Here, we present a near species-complete phylogeny of Cetartiodactyla based on cytochrome b sequence data. We evaluate the “reliability” of the phylogeny based on the recovery of numerous higher level benchmark clades and undisputed taxonomic groups. We argue that, at least for cytb within this group of mammals, dense taxon sampling may simultaneously overcome some of the commonly cited shortcomings of single-gene phylogenies and increase the value of the resulting phylogenies. We conclude that a profitable short-term research program will be the use of cytb data to rapidly provide species-level phylogenies for large clades across mammals providing valuable tools for comparative biology. Such phylogenies are not competing with character rich studies of relatively few taxa, nor with supertrees, but offer alternative tools, and ultimately will increase the power of supertree approaches to reconstruct even larger and better resolved “megatrees”.
Section snippets
Data and phylogenetic analyses
Cytochrome data was compiled from GenBank for 276 taxa representing 266 cetartiodactylans (including two recently extinct taxa, Myotragus balearicus, the ‘Mouse Goat’, and Megaloceros giganteus, the ‘Irish Elk’ or ‘Giant Deer’), and 10 outgroups (see Table 1 for Accession Nos.). We chose outgroup taxa representing two groups from Pegasoferae a recently proposed group hypothesized to be sister to Cetartiodactyla (Nishihara et al., 2006). Given that missing data can cause problems in phylogenetic
Benchmark clades
In the full dataset, all of the benchmark clades were recovered (Fig. 1, Fig. 2 and Table 2), except that one species Moschiola meminna, a member of Tragulidae grouped with Bovidae (Fig. 3), thereby rendering both families paraphyletic (according with current taxonomic classification). Moschiola has available sequence shorter than 30% (but slightly longer than 15%) of the full cytb sequence length is thus only included in the full matrix. In a subsequent analysis of the full matrix with this
Recovery of benchmark clades: the reliability of cytochrome b and importance of dense taxon sampling
Nearly all benchmark clades were recovered in all analyses (Fig. 1, Fig. 2, Fig. 3, Fig. 5 and Table 2). At the level of families the only real inconsistency surrounds a single species with a very short sequences available (Moschiola, Fig. 2). Otherwise, our results differ only from some traditional classifications in the placement of species whose phylogenetic position has been questioned by many previous studies (i.e. taxa that recent evidence suggests are misplaced in traditional
Conclusions
By analyzing a large number of cetartiodactylan species using a single mitochondrial gene our primary goal here is to provide a tool for species-level comparative studies. This approach offers rapid phylogenetic estimates for large clades, but may suffer by providing less reliable (less accurate) results than studies that include proportionally greater amount of character data. However, our results are, by and large, consistent with all major clades that can be treated as ‘known’ due to strong
Acknowledgments
Funding for this project came from a Slovenian Research Agency research fellowship (ARRS Z1-9799-0618-07) to Ingi Agnarsson, and Judith Parker Travel Grant, Lerner-Gray Fund for Marine Research of the American Museum of Natural History, Cetacean International Society, Latin American Student Field Research Award of the American Society of Mammalogists, Whale and Dolphin Conservation Society, the Russell E. Train Education Program-WWF, and FIU Dissertation Year Fellowship all to Laura
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Present address: Department of Biology, University of Puerto Rico, P.O. Box 23360, San Juan PR 00931-3360, USA.