A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla)

Despite the biological and economic importance of the Cetartiodactyla, the phylogeny of this clade remains controversial. Using the supertree approach of matrix representation with parsimony, we present the first phylogeny to include all 290 extant species of the Cetacea (whales and dolphins) and Artiodactyla (even-toed hoofed mammals). At the family-level, the supertree is fully resolved. For example, the relationships among the Ruminantia appear as (((Cervidae, Moschidae) Bovidae) (Giraffidae, Antilocapridae) Tragulidae). However, due to either lack of phylogenetic study or contradictory information, polytomies occur within the clades Sus, Muntiacus, Cervus, Delphinidae, Ziphiidae and Bovidae. Complete species-level phylogenies are necessary for both illustrating and analysing biological, geographical and ecological patterns in an evolutionary framework. The present species-level tree of the Cetartiodactyla provides the first opportunity to examine comparative hypotheses across entirely aquatic and terrestrial species within a single mammalian order.     

Subordinal artiodactyl relationships in the light of phylogenetic analysis of 12 mitochondrial protein-coding genes

Ursing, B. M., Slack, K. E. & Arnason, U. (2000) Subordinal artiodactyl relationships in the light of phylogenetic analysis of 12 mitochondrial protein-coding genes. — Zoologica Scripta , 29 , 83–88.
Extant artiodactyls (even-toed hoofed mammals) are traditionally divided into three main lineages: Suiformes (pigs, peccaries and hippopotamuses), Tylopoda (camels and llamas) and Ruminantia (bovids, deer, tragulids and giraffes). Recent molecular studies have not supported a close relationship between pigs and hippopotamuses, however, instead grouping hippopotamuses with Cetacea (whales, dolphins and porpoises). In this study we have sequenced the complete mitochondrial genome of a tylopod — the alpaca (Lama pacos), the only artiodactyl suborder not previously represented by a complete mitochondrial sequence. This sequence was included in phylogenetic analyses together with the complete mitochondrial protein-coding sequences of other artiodactyls plus two cetaceans. Despite the length of the data set, the relationship between Suina (Suiformes sine Hippopotamidae), Tylopoda and Ruminantia/Hippopotamidae/Cetacea could not be fully resolved, however, a basal position of the alpaca (Tylopoda) relative to the other artiodactyls/cetaceans was unsupported.     

Impact of increased character sampling on the phylogeny of Cetartiodactyla (Mammalia): combined analysis including fossils

The phylogenetic position of Cetacea (whales, dolphins and porpoises) is an important exemplar problem for combined data parsimony analyses because the clade is ancient and includes many well‐known and relatively complete fossil species. We combined data for 71 terminal taxa (43 extinct/28 extant) to test where Cetacea fits within Cetartiodactyla, and where various fossil hoofed mammals (e.g., ?entelodonts, “?anthracotheriids” and ?mesonychians) are positioned. We scored 635 phenotypic characters (osteology, dentition, soft tissue, behavior), approximately three times the number of characters in the last major analysis of this clade, and combined these with > 40 000 molecular characters, including new data from 10 genes. The analysis supported a topology consistent with the majority of recently published molecular studies. Cetacea was the extant sister taxon of Hippopotamidae, followed successively by Ruminantia, Suina and Camelidae. Several extinct taxa were phylogenetically unstable, upsetting resolution of the strict consensus and limiting branch support, but the positions of several key fossils were consistently resolved. The wholly extinct ?Mesonychia was more closely related to Cetacea than was any “artiodactylan.”“?Anthracotheriids” were paraphyletic, and, with the exception of one species, were more closely related to Hippopotamidae than to any other living taxon. The total evidence analysis overturned a highly nested position for Moschus supported by molecular data alone. The character partition that could be scored for the fossil taxa (osteological and dental characters) included more informative characters than most molecular partitions in our analysis, and had the fewest missing data. The osteological–dental data alone, however, did not support inclusion of cetaceans within crown “Artiodactyla.” Recently discovered ankle bones from fossil whales reinforced the monophyly of Cetartiodactyla but provided no particular evidence of derived similarities between hippopotamids and fossil cetaceans that were not shared with other “artiodactylans”. © The Willi Hennig Society 2007.     

Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes

The order Cetartiodactyla includes cetaceans (whales, dolphins and porpoises) that are found in all oceans and seas, as well as in some rivers, and artiodactyls (ruminants, pigs, peccaries, hippos, camels and llamas) that are present on all continents, except Antarctica and until recent invasions, Australia. There are currently 332 recognized cetartiodactyl species, which are classified into 132 genera and 22 families. Most phylogenetic studies have focused on deep relationships, and no comprehensive time-calibrated tree for the group has been published yet. In this study, 128 new complete mitochondrial genomes of Cetartiodactyla were sequenced and aligned with those extracted from nucleotide databases. Our alignment includes 14,902 unambiguously aligned nucleotide characters for 210 taxa, representing 183 species, 107 genera, and all cetartiodactyl families. Our mtDNA data produced a statistically robust tree, which is largely consistent with previous classifications. However, a few taxa were found to be para- or polyphyletic, including the family Balaenopteridae, as well as several genera and species. Accordingly, we propose several taxonomic changes in order to render the classification compatible with our molecular phylogeny. In some cases, the results can be interpreted as possible taxonomic misidentification or evidence for mtDNA introgression. The existence of three new cryptic species of Ruminantia should therefore be confirmed by further analyses using nuclear data. We estimate divergence times using Bayesian relaxed molecular clock models. The deepest nodes appeared very sensitive to prior assumptions leading to unreliable estimates, primarily because of the misleading effects of rate heterogeneity, saturation and divergent outgroups. In addition, we detected that Whippomorpha contains slow-evolving taxa, such as large whales and hippos, as well as fast-evolving taxa, such as river dolphins. Our results nevertheless indicate that the evolutionary history of cetartiodactyls was punctuated by four main phases of rapid radiation during the Cenozoic era: the sudden occurrence of the three extant lineages within Cetartiodactyla (Cetruminantia, Suina and Tylopoda); the basal diversification of Cetacea during the Early Oligocene; and two radiations that involve Cetacea and Pecora, one at the Oligocene/Miocene boundary and the other in the Middle Miocene. In addition, we show that the high species diversity now observed in the families Bovidae and Cervidae accumulated mainly during the Late Miocene and Plio-Pleistocene.     

The position of Cetacea within mammalia: phylogenetic analysis of morphological data from extinct and extant taxa

Knowledge of the phylogenetic position of the order Cetacea (whales, dolphins, and porpoises) within Mammalia is of central importance to evolutionary biologists studying the transformations of biological form and function that accompanied the shift from fully terrestrial to fully aquatic life in this clade. Phylogenies based on molecular data and those based on morphological data both place cetaceans among ungulates but are incongruent in other respects. Morphologists argue that cetaceans are most closely related to mesonychians, an extinct group of terrestrial ungulates. They have disagreed, however, as to whether Perissodactyla (odd-toed ungulates) or Artiodactyla (even-toed ungulates) is the extant clade most closely related to Cetacea, and have long maintained that each of these orders is monophyletic. The great majority of molecule-based phylogenies show, by contrast, not only that artiodactyls are the closest extant relatives of Cetacea, but also that Artiodactyla is paraphyletic unless cetaceans are nested within it, often as the sister group of hippopotamids. We tested morphological evidence for several hypotheses concerning the sister taxon relationships of Cetacea in a maximum parsimony analysis of 123 morphological characters from 10 extant and 30 extinct taxa. We advocate treating certain multistate characters as ordered because such a procedure incorporates information about hierarchical morphological transformation. In all most-parsimonious trees, whether multistate characters are ordered or unordered, Artiodactyla is the extant sister taxon of Cetacea. With certain multistate characters ordered, the extinct clade Mesonychia (Mesonychidae + Hapalodectidae) is the sister taxon of Cetacea, and Artiodactyla is monophyletic. When all fossils are removed from the analysis, Artiodactyla is paraphyletic with Cetacea nested inside, indicating that inclusion of mesonychians and other extinct stem taxa in a phylogenetic analysis of the ungulate clade is integral to the recovery of artiodactyl monophyly. Phylogenies derived from molecular data alone may risk recovering inconsistent branches because of an inability to sample extinct clades, which by a conservative estimate, amount to 89% of the ingroup. Addition of data from recently described astragali attributed to cetaceans does not overturn artiodactyl monophyly.     

The Phylogenetic Position of Cetaceans: Further Combined Data Analyses, Comparisons with the Stratigraphic Record and a Discussion of Character Optimization

A recent total evidence analysis of the position of cetaceans(whales, dolphins and porpoises and extinct relatives) amongmammals indicated that the phylogeny of these taxa remains poorlyresolved. Molecular data show that 1) the order Artiodactyla(even-toed ungulates) is paraphyletic unless whales are includedwithin it and 2) that the traditional relationships of cladeswithin Artiodactyla are not supported. This controversy alsoaffects the position of a wholly extinct clade, Mesonychia,which has been argued to be the group of terrestrial mammalsmost closely related to whales. Here I update a previous totalevidence analysis by adding several hundred new informativemolecular characters from the literature. Even with the additionof these characters the phylogeny remains unresolved. All mostparsimonious trees, however, indicate a paraphyletic Artiodactylawith conflict existing over the exact sister taxon of Cetacea.Congruence between different equally parsimonious cladogramsand the stratigraphic record as measured using the modifiedManhattan Stratigraphic Measure shows that all of the competingtopologies, including those with a paraphyletic Artiodactyla,are significantly congruent with the stratigraphic record. Infossil taxa cladistic optimization can be used as an alternativeto "argument from design" (Lauder, 1996) to reconstruct behaviorand soft tissues that do not fossilize or osteological charactersthat have not preserved. In certain scenarios of cetacean phylogeny,optimization indicates that taxa such as the archaic whalesAmbulocetus and Pakicetus, and possibly mesonychians, are morecorrectly reconstructed without hair.     

More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen

Recent phylogenetic analyses of DNA sequences suggest that cetaceans (whales) and hippopotamid artiodactyls (hippos) are extant sister taxa. Consequently, the shared aquatic specializations of these taxa may be synapomorphies. This molecular view is contradicted by paleontological data that overwhelmingly support a monophyletic Artiodactyla (even-toed ungulates) and a close relationship between Cetacea and extinct mesonychian ungulates. According to the fossil evidence, molecular, behavioral, and anatomical resemblances between hippos and whales are interpreted as convergences or primitive retentions. In this report, competing interpretations of whale origins are tested through phylogenetic analyses of the blood-clotting protein gene gamma- fibrinogen from cetaceans, artiodactyls, perissodactyls (odd-toed ungulates), and carnivores (cats, dogs, and kin). In combination with published DNA sequences, the gamma-fibrinogen data unambiguously support a hippo/whale clade and are inconsistent with the paleontological perspective. If the phylogeny favored by fossil evidence is accepted, the convergence at the DNA level between Cetacea and Hippopotamidae is remarkable in its distribution across three genetic loci: gamma-fibrinogen, the linked milk casein genes, and mitochondrial cytochrome b.      

Bayesian inference of cetacean phylogeny based on mitochondrial genomes

The phylogeny of Cetacea (whales, dolphins, porpoises) has long attracted the interests of biologists and has been investigated by many researchers based on different datasets. However, some phylogenetic relationships within Cetacea still remain controversial. In this study, Bayesian analyses were performed to infer the phylogeny of 25 representative species within Cetacea based on their mitochondrial genomes for the first time. The analyses recovered the clades resolved by the previous studies and strongly supported most of the current cetacean classifications, such as the monophyly of Odontoceti (toothed whales) and Mysticeti (baleen whales). The analyses provided a reliable and comprehensive phylogeny of Cetacea which can provide a foundation for further exploration of cetacean ecology, conservation and biology. The results also showed that: (i) the mitochondrial genomes were very informative for inferring phylogeny of Cetacea; and (ii) the Bayesian analyses outperformed other phylogenetic methods on inferring mitochondrial genome-based phylogeny of Cetacea.     

Stability of cladistic relationships between Cetacea and higher-level artiodactyl taxa

Over the past 10 years, the phylogenetic relationships among higher-level artiodactyl taxa have been examined with multiple data sets. Many of these data sets suggest that Artiodactyla (even-toed ungulates) is paraphyletic and that Cetacea (whales) represents a highly derived "artiodactyl" subgroup. In this report, phylogenetic relationships between Cetacea and artiodactyls are tested with a combination of 15 published data sets plus new DNA sequence data from two nuclear loci, interphotoreceptor retinoid-binding protein (IRBP) and von Willebrand factor (vWF). The addition of the IRBP and vWF character sets disrupts none of the relationships supported by recent cladistic analyses of the other 15 data sets. Simultaneous analyses support three critical clades: (Cetacea + Hippopotamidae), (Cetacea + Hippopotamidae + Ruminantia), and (Cetacea + Hippopotamidae + Ruminantia + Suina). Perturbations of the combined matrix show that the above clades are stable to a variety of disturbances. A chronicle of phylogenetic results over the past 3 years suggests that cladistic relationships between Cetacea and artiodactyls have been stable to increased taxonomic sampling and to the addition of more than 1,400 informative characters from 15 data sets.     

On the origin of Cetartiodactyla: Comparison of data on evolutionary morphology and Molecular biology

The data on phylogeny and early evolution of Cetartiodactyla are analyzed and a model for the initial stage of their history is proposed. It is shown that the roots of Cetartiodactyla go back to generalized Cretaceous terrestrial Eutheria, and a hypothetical basal group of Cetartiodactyla was probably ancestral to the orders Artiodactyla and Cetacea. The Artiodactyla-Cetacea divergence and adaptive radiation of Artiodactyla, which gave rise to the suborders Ruminantia, Tylopoda, and Suiformes, apparently occurred in the pre-Eocene time, earlier than 55 Ma. Molecular similarity between Hippopotamidae and Cetacea is evidence of common origin of Artiodactyla and Cetacea and adaptation to aquatic environment.     

From Land to Water: the Origin of Whales, Dolphins, and Porpoises

Cetaceans (whales, dolphins, and porpoises) are an order of mammals that originated about 50 million years ago in the Eocene epoch. Even though all modern cetaceans are obligate aquatic mammals, early cetaceans were amphibious, and their ancestors were terrestrial artiodactyls, similar to small deer. The transition from land to water is documented by a series of intermediate fossils, many of which are known from India and Pakistan. We review raoellid artiodactyls, as well as the earliest families of cetaceans: pakicetids, ambulocetids, remingtonocetids, protocetids, and basilosaurids. We focus on the evolution of cetacean organ systems, as these document the transition from land to water in detail.     

Identification and characterization of a tandem repeat in exon III of the dopamine receptor D4 (DRD4) gene in cetaceans

A large number of mammalian species harbor a tandem repeat in exon III of the gene encoding dopamine receptor D4 (DRD4), a receptor associated with cognitive functions. In this study, a DRD4 gene exon III tandem repeat from the order Cetacea was identified and characterized. Included in our study were samples from 10 white-beaked dolphins (Lagenorhynchus albirostris), 10 harbor porpoises (Phocoena phocoena), eight sperm whales (Physeter macrocephalus), and five minke whales (Balaenoptera acutorostrata). Using enzymatic amplification followed by sequencing of amplified fragments, a tandem repeat composed of 18-bp basic units was detected in all of these species. The tandem repeats in white-beaked dolphin and harbor porpoise were both monomorphic and consisted of 11 and 12 basic units, respectively. In contrast, the sperm whale harbored a polymorphic tandem repeat with size variants composed of three, four, and five basic units. Also the tandem repeat in minke whale was polymorphic; size variants composed of 6 or 11 basic units were found in this species. The consensus sequences of the basic units were identical in the closely related white-beaked dolphin and harbor porpoise, and these sequences differed by a maximum of two changes when compared to the remaining species. There was a high degree of similarity between the cetacean basic unit consensus sequences and those from members of the horse family and domestic cow, which also harbor a tandem repeat composed of 18-bp basic units in exon III of their DRD4 gene. Consequently, the 18-bp tandem repeat appears to have originated prior to the differentiation of hoofed mammals into odd-toed and even-toed ungulates. The composition of the tandem repeat in cetaceans differed markedly from that in primates, which is composed of 48-bp repeat basic units.     

A phylogenetic blueprint for a modern whale

The emergence of Cetacea in the Paleogene represents one of the most profound macroevolutionary transitions within Mammalia. The move from a terrestrial habitat to a committed aquatic lifestyle engendered wholesale changes in anatomy, physiology, and behavior. The results of this remarkable transformation are extant whales that include the largest, biggest brained, fastest swimming, loudest, deepest diving mammals, some of which can detect prey with a sophisticated echolocation system (Odontoceti – toothed whales), and others that batch feed using racks of baleen (Mysticeti – baleen whales). A broad-scale reconstruction of the evolutionary remodeling that culminated in extant cetaceans has not yet been based on integration of genomic and paleontological information. Here, we first place Cetacea relative to extant mammalian diversity, and assess the distribution of support among molecular datasets for relationships within Artiodactyla (even-toed ungulates, including Cetacea). We then merge trees derived from three large concatenations of molecular and fossil data to yield a composite hypothesis that encompasses many critical events in the evolutionary history of Cetacea. By combining diverse evidence, we infer a phylogenetic blueprint that outlines the stepwise evolutionary development of modern whales. This hypothesis represents a starting point for more detailed, comprehensive phylogenetic reconstructions in the future, and also highlights the synergistic interaction between modern (genomic) and traditional (morphological + paleontological) approaches that ultimately must be exploited to provide a rich understanding of evolutionary history across the entire tree of Life.     

Phylogenomic analyses and improved resolution of Cetartiodactyla

The remarkable antiquity, diversity, and significance in the ecology and evolution of Cetartiodactyla have inspired numerous attempts to resolve their phylogenetic relationships. However, previous analyses based on limited samples of nuclear genes or mitochondrial DNA sequences have generated results that were either inconsistent with one another, weakly supported, or highly sensitive to analytical conditions. Here, we present strongly supported results based upon over 1.4 Mb of an aligned DNA sequence matrix from 110 single-copy nuclear protein-coding genes of 21 Cetartiodactyla species, which represent major Cetartiodactyla lineages, and three species of Perissodactyla and Carnivora as outgroups. Phylogenetic analysis of this newly developed genomic sequence data using a codon-based model and recently developed models of the rate autocorrelation resolved the phylogenetic relationships of the major cetartiodactylan lineages and of those lineages with a high degree of confidence. Cetacea was found to nest within Artiodactyla as the sister group of Hippopotamidae, and Tylopoda was corroborated as the sole base clade of Cetartiodactyla. Within Cetacea, the monophyletic status of Odontoceti relative to Mysticeti, the basal position of Physeteroidea in Odontoceti, the non-monophyly of the river dolphins, and the sister relationship between Delphinidae and Monodontidae + Phocoenidae were strongly supported. In particular, the groups of Tursiops (bottlenose dolphins) and Stenella (spotted dolphins) were validated as unnatural groups. Additionally, a very narrow time frame of ∼3 My (million years) was found for the rapid diversification of delphinids in the late Miocene, which made it difficult to resolve the phylogenetic relationships within the Delphinidae, especially for previous studies with limited data sets. The present study provides a statistically well-supported phylogenetic framework of Cetartiodactyla, which represents an important step toward ending some of the often-heated, century-long debate on their evolution.     

Hunting to extinction: biology and regional economy influence extinction risk and the impact of hunting in artiodactyls

Half of all artiodactyls (even-toed hoofed mammals) are threatened with extinction, around double the mammalian average. Here, using a complete species-level phylogeny, we construct a multivariate model to assess for the first time which intrinsic (biological) and extrinsic (anthropogenic and environmental) factors influence variation in extinction risk in artiodactyls. Globally artiodactyls at greatest risk live in economically less developed areas, have older weaning ages and smaller geographical ranges. Our findings suggest that identifying predictors of threat is complicated by interactions between both biological and anthropogenic factors, resulting in differential responses to threatening processes. Artiodactyl species that experience unregulated hunting live in significantly less economically developed areas than those that are not hunted; however, hunted species are more susceptible to extinction if they have slower reproductive rates (older weaning ages). In contrast, risk in non-hunted artiodactyls is unrelated to reproductive rate and more closely associated with the economic development of the region in which they live.     

What can dolphins tell us about primate evolution?

Fifty-five million years ago, a furry, hoofed mammal about the size of a dog ventured into the shallow brackish remnant of the Tethys Sea and set its descendants on a path that would lead to their complete abandonment of the land. These early ancestors of cetaceans (dolphins, porpoises, and whales) thereafter set on an evolutionary course that is arguably the most unusual of any mammal that ever lived. Primates and cetaceans, because of their adaptation to exclusively different physical environments, have had essentially nothing to do with each other throughout their evolution as distinct orders. In fact, the closest phylogenetic relatives of cetaceans are even-toed ungulates.     

Ecological evolution of early Cetartiodactyla and reconstruction of its missing initial link

The analysis of biodiversity and ecological evolution of Eocene Cetartiodactyla against the background of changes in the biosphere, biota, and paleogeography has provided a model for the origin, development, and dispersal of this group. The main trends in ecogenesis, occurrence data, relationships between the main evolutionary events and great abiotic and biotic events are considered and the possibility of Cretaceous origin of Cetartiodactyla is corroborated. Cetartiodactyla could have arise in the Late Cretaceous in Asia south of 30°–40° N or in the southern Indochina Peninsula; they diverged very early into Cetacea and Artiodactyla. The model proposed confirms monophyly of Cetartiodactyla, Artiodactyla, and Cetacea. The existence of a missing initial link explains considerable changes in the Archaeoceti structure (in particular, dentition), as compared to that of Artiodactyla. Eocene Artiodactyla were closer in ecology to the initial type of Cretaceous Eutheria.     

Parsimony Analysis of Total Evidence from Extinct and Extant Taxa and the Cetacean-Artiodactyl Question (Mammalia, Ungulata)

Many molecule-based phylogenetic analyses find that the mammalian order Artiodactyla (even-toed ungulates) is paraphyletic unless cetaceans (whales, dolphins, and porpoises) are nested within it, a hypothesis that runs contrary to traditional morphology-based ideas. Here I present a total evidence analysis of this question based on 10 extant and 27 extinct taxa, using two character data partitions: (i) skeletal data and (ii) neontological data (soft morphology, retroposons, and DNA sequences [γ-fibrinogen, β-casein, and κ-casein and mt cytochrome b ]). A sensitivity analysis varying gap cost and transversion/transition ratio over nine parameters was implemented in the sequence alignment and in the parsimony analysis. The two data partitions are significantly incongruent, and the neontological data partition includes over six times as many characters as the osteological data partition. The osteological data partition, however, samples almost three times more taxa, taxa that cannot be sampled for neontological data because they are extinct. Osteological data resulted in artiodactyl monophyly, and neontological data resulted in artiodactyl paraphyly over all nine parameters. In the total evidence analysis the parameter most congruent with the overall character data is unresolved as to the sister taxon of Cetacea; however, the Adams consensus tree favors the neontological result. Extinction of almost 90% of the clade and particularly poor knowledge of stem taxa at the base of Artiodactyla make resolution of conflicting molecule- and morphology-based phylogenetic signals particularly difficult.     

On the Unnecessary and Misleading Taxon “Cetartiodactyla”

Journal of Mammalian Evolution - The name “Cetartiodactyla” was proposed in 1997 to reflect the molecular data that suggested that Cetacea is closely related to Artiodactyla. Since...