Assembling the Ruminant Tree: Combining Morphology, Molecules, Extant Taxa, and Fossils
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Zitteliana B 32 (2014) 197 Assembling the ruminant tree: combining morphology, molecules, extant taxa, and fossils Faysal Bibi Department of Mammalogy, American Museum of Natural History, New York NY 10024, USA. Zitteliana B 32, 197 – 211 Current address: Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, München, 31.12.2014 Invalidenstr 43, Berlin 10115, Germany. E-mail: [email protected] Manuscript received 01.04.2014; revision accepted 22.09.2014 ISSN 1612 - 4138 Abstract A gap exists between paleontological and neontological approaches to ruminant phylogenetics, despite great increases in phyloge- netic resolution through molecular work of the last three decades, and a large and growing fossil record. This gap is reflected in differing methodological approaches, with insufficient integration of the large fossil record by molecular studies on the one hand, and insufficient consideration of highly resolved genomic work by paleontological studies on the other. Both paleontological and molecular approaches seek to answer similar broad evolutionary questions, and a synthetic approach is in the interest of all. I demonstrate this by reviewing the development of each field, noting many examples in which paleontological or molecular approaches to ruminant phylogenetics are, on their own, inadequate compared to an approach which considers all sources of data together. In particular, cases such as those of Bison, Capra, and Pelea have shown that integration of genomic and anatomical data presents better resolution of relationships, and I suggest Antilocapra and Moschus may benefit from a similar approach, especially with the integration of fossil taxa into a combined (supermatrix) analysis. I present preliminary results of a new and large (in progress) morphological matrix that is intended to be used for the incorpo- ration of anatomical data and fossil taxa into a combined analysis. The new matrix is much larger than previous morphological matrices assembled for ruminant phylogenetics, meaning it can support a larger number of fossil taxa than was previously possible. Preliminary analysis with 18 taxa recovers a highly supported tree that is mostly compatible with both traditional and molecular phylogenies, alt- hough problems of convergence remain, such as between Antilocapra and Bovidae. Finally, I propose standardization of ruminant clade names in order to limit miscommunication between paleontological and neontological workers. I propose phylogenetic definitions based on crown (extant) clades for the names Ruminantia and Pecora, and the use of Pan-Ruminantia and Pan-Pecora to accommodate each respective crown clade plus its stem group. Key words: Ruminantia, phylogeny, total evidence, Bovidae. 1. Introduction large-scale questions of evolution, biogeography, and ecology. In 1968, Alan Gentry published a letter in Na- Early molecular papers of the 1980s and 1990s ture challenging the constancy of modern biogeo- would regularly cite these and other ecological or graphic boundaries into the deep past based on a paleontological papers. Today, however, it seems study of the bovid fossil record. A few years later, that many molecular investigations into ruminant Elisabeth Vrba published two papers presenting phylogenetics make little to no reference to the fos- the chronology and ecology of important hominid sil record, and paleontological studies on ruminants sites South Africa, also through the bovid fossil re- too often make no mention whatsoever (whether cord, and also in the pages of Nature (Vrba 1974; to support or challenge) of the results of the many Vrba 1975). Though studies and descriptions of ru- molecular phylogenetic advances of the last two minants both living and fossil already had an esta- decades. In that vein, the first International Confe- blished scientific history (e.g. Frick 1937; Lydekker rence on Ruminant Phylogenetics was held in Mu- 1898; Pilgrim 1947), these may have been the first nich in September 2013, bringing together over and clearest demonstrations, in such a widely read fifty specialists from around the world with diverse journal, of the power of a diverse and widespread interests in the anatomy, physiology, ecology, bi- clade of ruminants to directly address and resolve ogeography, phylogenetics, ontogeny, behavior, Zitteliana B 32 (2014) 198 genomics, and fossil record of ruminant species The floodgates opened in the mid to late 90s, with (Rössner 2013). This conference was timely, given an explosion of molecular phylogenetic work on all the massive increases in phylogenetic information of aspects of life, tracking technological improvements the last two decades, and the need to develop an allowing faster sequencing of ever longer portions integrative approach to ruminant phylogenetics. of genomes from ever greater numbers of taxa. Ru- The goal of the current paper is to present a sum- minant phylogenetics, but especially that of bovids, mary of accomplishments to date in ruminant phylo- greatly profited. Monophyly of Pecora, and of the five genetic work and to present some preliminary data pecoran families (Antilocapridae, Bovidae, Cervidae, from ongoing work. This includes outlooks for future Giraffidae, Moschidae), was supported throughout progress, especially for combining data from extant (e.g. Cronin et al. 1996; Randi et al. 1998), though taxa and molecular work with that from fossil taxa the exact relationships among these families conti- and morphological studies. I will also present preli- nued to elude satisfactory resolution (and arguably minary results of a new large skeletal morphological still do). In fact, early on it was recognized that the dataset (matrix) intended for use in combined (super- poor resolution at the base of Pecora probably re- matrix) phylogenetic analyses. Bovids make up some flected rapid cladogenesis as a result of an adap- two-thirds of all ruminants, so the focus of much of tive radiation early in the clade’s history (Hassanin & the work reviewed here is based on this clade. Douzery 2003; Kraus & Miyamoto 1991). Within Cervidae, the monophyly of morphological- 2.1 Molecular Phylogenetics ly defined clades Cervinae (aka Plesiometacarpalia, Old World deer) and Capreolinae (aka Odocoilein- Domestic animals, especially goats, sheep, and ae, Telemetacarpalia, or New World deer) was sup- cattle, form an essential economic and dietary com- ported, while the antlerless water deer (Hydropotes) ponent of human societies around the world. As a was found to be sister to roe deer (Capreolus) and result, studies into the biology of these animals are close to Capreolinae, partly supporting the propo- common, from anatomical and veterinary works of sal of Bouvrain et al. (1989) and contradicting others centuries past, to physiological and histological in- based on morphological grounds (Cronin et al. 1996; vestigations of the twentieth century. With the disco- Gilbert et al. 2006; Pitra et al. 2004; Randi et al. very of nuclear cell structures, chromosomal investi- 1998; Randi et al. 2001). The molecular phylogenetic gations in the 1960s and 1970s began to investigate placement of Antilocapra as basal to all remaining phylogenetic relationships directly, giving some in- pecorans (Cronin et al. 1996; Hassanin & Douzery dication of the power of molecules to resolve rela- 2003) was also something of a surprise, rather than tionships from the level of populations upwards to it being more closely related to cervids or bovids as entire phyla (e.g. Buckland & Evans 1978; Wurster & had often been proposed (Gentry & Hooker 1988; Benirschke 1968). With the development of immu- Janis & Scott 1987). nological distance techniques, Lowenstein (1986) Within Bovidae, we have seen confirmation of constructed a molecular tree of Bovidae, substantia- Kingdon’s (1982) hypothesis of a basal split of ting a basal split of bovids into two major subclades. this clade into Bovinae and Antilopinae (Gatesy et This supported (unknowingly it seems) a phylogene- al. 1997; Gatesy et al. 1992; Hassanin & Douze- tic tree that Kingdon (1982) had proposed four years ry 1999b; Lowenstein 1986; Matthee & Robinson earlier on the basis of ecological and morphological 1999); the polyphyletic status of ‘Neotragini’ and its features. In an early example of the molecular clock, inclusion into a larger Antilopini clade (Georgiadis et Lowenstein also estimated the origins of crown Bo- al. 1990; Rebholz & Harley 1999); a total reorganiza- vidae at around 25 Ma, a surprisingly good assess- tion of the clades within Caprini (formerly Caprinae) ment for the time. (Groves & Shields 1996; Hassanin et al. 1998; Ropi- Mitochondrial DNA (mtDNA) sequencing threw quet & Hassanin 2005); clarification of genus-level open the doors for a genomic phylogenetic revoluti- clades among Antilopini (Nanger, Eudorcas, Gazella, on that continues to this day. An early examination of etc.) (Bärmann et al. 2013), Cephalophini (van Vu- the mtDNA of Bovini (Miyamoto et al. 1989) recove- uren & Robinson 2001), Bovini (Hassanin et al. 2013; red initial molecular support for a deep split between Miyamoto et al. 1989), Tragelaphini (Moodley et al. Bovina (oxen: Bos spp.) and Bubalina (buffaloes: Bu- 2009; Willows-Munro et al. 2005), and Reduncini (Bi- balus, Syncerus), and the synonymy of Bison with rungi & Arctander 2001; Cotterill 2005); placement of Bos (supporting previous suggestions by van Gelder some of the most enigmatic taxa including the rhe- 1977, Gentry 1978, Groves 1981, and others). Broa-