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Whales and Even-Toed Ungulates (Cetartiodactyla)

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Whales and Even-Toed Ungulates (Cetartiodactyla) Whales and even-toed ungulates (Cetartiodactyla) John Gatesy 7 e systematic database for Cetartiodactyla is large. Department of Biology, University of California, Riverside, CA 92521, Nuclear genome sequences are completed or in progress USA ([email protected]) for members of four cetartiodactyl families. Mitochon- drial (mt) genomes have been sequenced from 18 fam- ilies (11, 13, 15), insertions of transposons have been Abstract scored from most families (7, 16, 17), and cladistic ana- Whales and even-toed ungulates are grouped into ~24 lysis of paleontological data sets is at an advanced stage families within the mammalian Order Cetartiodactyla. (18–25). Perhaps most importantly, several large matrices Recent phylogenetic analyses of molecular and morpho- of fossil and molecular data have been compiled (26–29). logical data robustly support most interfamilial relation- Studies based on these combined data sets permit direct ships, including a nested position of whales within the synthesis of DNA sequence data with temporal informa- order. However, resolution among basal clades of toothed tion from the fossil and geological record. whales and groupings within Ruminantia remain elusive. Given the wealth of systematic evidence, there are The fossil record of Cetartiodactyla is rich and has inspired some areas of strong congruence between analyses of many molecular clock studies. The cetartiodactyl timetree morphological and molecular data sets. Suina, a grouping suggests that the earliest divergences among living species of Suidae (pigs) and Tayassuidae (peccaries), is robustly may have occurred in the Cretaceous (146–66 million years supported by both DNA sequences and phenotypic char- ago, Ma) and that the majority of splits among families were acters (3, 14, 16, 20, 23–25, 27, 28, 30–33 ). Likewise, a in the Oligocene (34–23 Ma). cluster of species that “chew the cud,” Ruminantia, has been consistently supported by diverse analyses, in com- Whales (Cetacea) and even-toed ungulates (“Artiodac- bination with Pecora, a subclade of Ruminantia (3, 9, 14, tyla,” not a natural group) are represented by ~290 extant 16, 18, 20, 23, 27, 28, 30–35). Pecora includes all extant species (1), and have been grouped into 20–25 families cetartiodactylans with prominent cranial appendages within the placental Order Cetartiodactyla (Fig. 1). (Bovidae = antelopes and cattle, Cervidae = antlered deer, Extinct diversity is well represented in the clade, with Gira1 dae = giraB es, and Antilocapridae = pronghorn about six extinct genera for every genus that contains extant species (2). 7 is rich fossil record has facilitated molecular clock analyses (3–14), but phenotypic diversity in the group is extensive and has confounded systematic studies. Cetartiodactylans range in body size from the tiny ~4 kg mouse deer, Tragulus javanicus, to the enor- mous 190,000 kg Blue Whale, Balaenoptera musculus (1). It is oJ en di1 cult to assess homology of structures in organisms that are as divergent as these in terms of ana- tomical organization, mass, and ecological specializa- tion. Among taxa with living representatives, McKenna and Bell (2) recognized 11 families of Cetacea and 10 families of “Artiodactyla.” 7 ree additional family-level groups (Eschrichtiidae, Neobalaenidae, and Kogiidae) are commonly accepted. Here I review the phylogen- Fig. 1 An antilocaprid (Antilocapra americana; foreground) and etic relationships and divergence times of the families of a bovid (Bison bison; background). Credit: painting by C. Buell Cetartiodactyla (Fig. 2). (J. Gatesy, copyright). J. Gatesy. Whales and even-toed ungulates (Cetartiodactyla). Pp. 511–515 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 551111 11/28/2009/28/2009 11:30:29:30:29 PPMM 512 THE TIMETREE OF LIFE Monodontidae 23 21 Phocoenidae Delphinidae 16 Iniidae 20 Pontoporiidae 12 19 Lipotidae 11 Hyperoodontidae Odontoceti Platanistidae 9 Cetacea Kogiidae 17 Physeteridae 7 Balaenopteridae 22 18 Eschrichtiidae 4 14 Neobalaenidae Mysticeti Balaenidae Hippopotamidae Bovidae 3 15 Moschidae 13 Cervidae 10 8 Giraffidae 2 Ruminantia 5 Antilocapridae Tragulidae "Artiodactyla" 1 Suidae 6 Tayassuidae Suina Camelidae Paleogene Neogene CENOZOIC 50 25 0 Million years ago Fig. 2 A timetree of whales and even-toed ungulates (Cetartiodactyla). Divergence times are shown in Table 1. Hyperoodontidae = Ziphiidae. antelopes), as well Moschidae (musk deer), which may Despite this consensus, sharp conP icts between mol- be hornless primitively (28) or secondarily (9, 18). DNA ecules and morphology have emerged over the past data and the phenotypic evidence also generally agree 20 years. Non-monophyly of “Artiodactyla,” even-toed in supporting Cetacea (whales), Odontoceti (toothed ungulates, is perhaps the most striking molecular incon- whales), Mysticeti (baleen whales), Eschrichtiidae (Gray gruence with traditional mammalian taxonomy. Mul- Whale) + Balaenopteridae (rorqual baleen whales), tiple nuclear gene sequences (5, 6, 10, 30, 31), mt genomes Physeteroidea (Physeteridae = Giant Sperm Whale and (11), and insertions of transposons (16) support a close Kogiidae = Dwarf and Pygmy Sperm Whales), Iniidae relationship between Cetacea and Hippopotamidae (Amazon River Dolphin) + Pontoporiidae (Franciscana (hippos), which is closest to Ruminantia (Fig. 2). 7 e Dolphin), and Delphinoidea (Delphinidae = oceanic dol- clusters render “Artiodactyla” paraphyletic, in contrast phins, Phocoenidae = porpoises, and Monodontidae = to most cladistic analyses of phenotypic data that favor Beluga and Narwhal) (4–8, 10, 11, 13–17, 19, 20, 22, 23, a monophyletic grouping of even-toed ungulates (20, 21, 26–33, 36, 37). 25, 28; but see 23, 24). Recently discovered hindlimbs HHedges.indbedges.indb 551212 11/28/2009/28/2009 11:30:31:30:31 PPMM HHedges.indb 513 e d g e s . i n d b 5 1 3 Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among whales and even-toed ungulates (Cetartiodactyla). Timetree Estimates Node Time Refs. (3, 11) Ref. (4) Refs. (7, 9) Ref. (8)(a) Ref. (8)(b) Ref. (10)(a) Ref. (10)(b) Refs. (13, 14) Time Time CI Time CI Time CI Time CI Time CI Time CI Time CI 167.3– ––––67.373–6364.168–6063.865–6255.360–5174.177–71 263.5– ––––63.568–5962.566–5760.562–5950.756–4671.674–70 359.1– ––––59.163–5557.763–5555.757–5444.149–3965.968–63 452.953.3––––52.955–5252.955–5252.454–5239.845–3559.562–57 546.3– ––46.355–39–––––––––– 642.842.8––––––––––––49.764–36 7 32.3 – 47.5 54–42 32.3 37–27 27.4 33–22 25.5 31–22 29.6 34–25 20.3 25–16 – – 831.6– ––31.636–28–––––––––– 930.032.145.551–4130.035–25–––––––––– 1029.4– ––29.433–2622.028–17–––––––– 1128.9– ––28.934–24–––––––––– 1228.2– ––28.233–23–––––––––– 1327.8– ––27.830–25–––––––––– 1427.320.931.036–26––––––––––27.329–25 1526.2– ––26.229–24–––––––––– 1625.022.4––25.030–20–––––––––– 1724.524.537.042–32–––––––––––– 1823.317.6––––––––––––23.326–21 1921.5– – 21.526–17–––––––––– 2019.918.423.026–2019.924–16–––––––––– 2119.81624.528–2219.824–16–––––––––– 2219.314.721.526–18––––––––––19.322–16 23 13.1 12.8 20.0 22–18 13.1 17–9 – – – – – – – – – – Note: Node times in the timetree are from refs. (3, 7, 8(a), 9, 11, 13). For ref. (8), times are included from (a) Bayesian analysis of mitochondrial and nuclear DNA from ref. (5), and (b) Bayesian analysis of mitochondrial genome data translated into amino acids. For ref. (10), times are included from (a) Bayesian analysis of mitochondrial and nuclear DNA from ref. (6) using all calibrations, and (b) Bayesian analysis of mitochondrial and nuclear DNA from ref. (6) using all calibrations except those within Cetartiodactyla. 11/28/2009 1:30:31 PM / 2 8 / 2 0 0 9 1 : 3 0 : 3 1 P M 514 THE TIMETREE OF LIFE from Eocene whales (21, 38) show that early cetaceans that much of the splitting among cetartiodactyl families had a paraxonic tarsus with a typical “artiodactyl” (12 of 23 divergences) occurred in the Oligocene. 7 ese ankle (39), but such characters provide support for a divergences include the di1 cult-to-resolve radiations at grouping of Cetacea with “Artiodactyla,” but not within the base of Odontoceti and at the base of Pecora (Fig. 2). “Artiodact yla” (21, 25, 28). Additional conP icts between 7 e 95% credibility intervals for estimates of diver- morphology and molecules include monophyly vs. para- gence times among all A ve pecoran families overlap, phyly of Balaenoidea (Balaenidae = right whales and and speciation events that separate odontocete families Neobalaenidae = Pygmy Right Whale) (11, 13, 15, 17, 22, also are tightly spaced in time. 7 e earliest branching 29, 37), monophyly vs. non-monophyly of Phocoenidae + point within Cetartiodactyla predates the Cretaceous/ Monodontidae (4, 7, 11, 15, 22, 28, 32, 36), monophyly Paleocene boundary in the timetree, but alternative ana- vs. polyphyly of river dolphins (Iniidae, Pontoporiidae, lyses push multiple nodes to the Cretaceous (14) or restrict Lipotidae = Chinese River Dolphin, and Platanistidae = all nodes to the Cenozoic (66–0 Ma) (10), depending on Indian River Dolphin) (4, 7, 11, 15, 22), monophyly vs. choice of fossil constraints, database, and methodology. polyphyly of Selenodontia (Ruminantia and Cameli- Molecular clock analyses within Cetartiodactyla dae = camels), and monophyly vs. non-monophyly of have been common, in part because extinct taxa have Suiformes (Suina and Hippopotamidae) (3, 5, 6, 10, 11, been directly integrated into cladistic studies, and also 16, 20, 21, 23, 25, 28, 30–32). Molecular resolutions of because extensive genetic data have been compiled for these conP icts are shown in Fig. 2. members of this group. However, even with this eB ort, Neither separate nor combined systematic matri- critical ambiguities remain. For example, the diver- ces have robustly resolved some interfamilial relation- gence of Cetacea from other cetartiodactylans is a very ships within Cetartiodactyla.
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