A new fossil species supports an early origin for toothed whale echolocation.

Odontocetes (toothed whales, dolphins and porpoises) hunt and navigate through dark and turbid aquatic environments using echolocation; a key adaptation that relies on the same principles as sonar. Among echolocating vertebrates, odontocetes are unique in producing high-frequency vocalizations at the phonic lips, a constriction in the nasal passages just beneath the blowhole, and then using air sinuses and the melon to modulate their transmission. All extant odontocetes seem to echolocate; however, exactly when and how this complex behaviour--and its underlying anatomy--evolved is largely unknown. Here we report an odontocete fossil, Oligocene in age (approximately 28 Myr ago), from South Carolina (Cotylocara macei, gen. et sp. nov.) that has several features suggestive of echolocation: a dense, thick and downturned rostrum; air sac fossae; cranial asymmetry; and exceptionally broad maxillae. Our phylogenetic analysis places Cotylocara in a basal clade of odontocetes, leading us to infer that a rudimentary form of echolocation evolved in the early Oligocene, shortly after odontocetes diverged from the ancestors of filter-feeding whales (mysticetes). This was followed by enlargement of the facial muscles that modulate echolocation calls, which in turn led to marked, convergent changes in skull shape in the ancestors of Cotylocara, and in the lineage leading to extant odontocetes.

Evidence for convergent evolution of ultrasonic hearing in toothed whales (Cetacea: Odontoceti).

Toothed whales (Cetacea: Odontoceti) are the most diverse group of modern cetaceans, originating during the Eocene/Oligocene transition approximately 38 Ma. All extant odontocetes echolocate; a single origin for this behaviour is supported by a unique facial source for ultrasonic vocalizations and a cochlea adapted for hearing the corresponding echoes. The craniofacial and inner ear morphology of Oligocene odontocetes support a rapid (less than 5 Myr) early evolution of echolocation. Although some cranial features in the stem odontocetes Simocetus and Olympicetus suggest an ability to generate ultrasonic sound, until now, the bony labyrinths of taxa of this grade have not been investigated. Here, we use µCT to examine a petrosal of a taxon with clear similarities to Olympicetus avitus. Measurements of the bony labyrinth, when added to an extensive dataset of cetartiodactyls, resulted in this specimen sharing a morphospace with stem whales, suggesting a transitional inner ear. This discovery implies that either the lineage leading to this Olympicetus--like taxon lost the ability to hear ultrasonic sound, or adaptations for ultrasonic hearing evolved twice, once in xenorophids and again on the stem of the odontocete crown group. We favour the latter interpretation as it matches a well-documented convergence of craniofacial morphology between xenorophids and extant odontocetes.

A toothless dwarf dolphin (Odontoceti: Xenorophidae) points to explosive feeding diversification of modern whales (Neoceti).

Toothed whales (Odontoceti) are adapted for catching prey underwater and possess some of the most derived feeding specializations of all mammals, including the loss of milk teeth (monophyodonty), high tooth count (polydonty), and the loss of discrete tooth classes (homodonty). Many extant odontocetes possess some combination of short, broad rostra, reduced tooth counts, fleshy lips, and enlarged hyoid bones-all adaptations for suction feeding upon fishes and squid. We report a new fossil odontocete from the Oligocene (approx. 30 Ma) of South Carolina (Inermorostrum xenops, gen. et sp. nov.) that possesses adaptations for suction feeding: toothlessness and a shortened rostrum (brevirostry). Enlarged foramina on the rostrum suggest the presence of enlarged lips or perhaps vibrissae. Phylogenetic analysis firmly places Inermorostrum within the Xenorophidae, an early diverging odontocete clade typified by long-snouted, heterodont dolphins. Inermorostrum is the earliest obligate suction feeder within the Odontoceti, a feeding mode that independently evolved several times within the clade. Analysis of macroevolutionary trends in rostral shape indicate stabilizing selection around an optimum rostral shape over the course of odontocete evolution, and a post-Eocene explosion in feeding morphology, heralding the diversity of feeding behaviour among modern Odontoceti.

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.

The origins of the killer whale ecomorph.

The killer whale (Orcinus orca) and false killer whale (Pseudorca crassidens) are the only extant cetaceans that hunt other marine mammals, with pods of the former routinely preying on baleen whales >10 m in length and the latter being known to take other delphinids.1-3 Fossil evidence for the origins of this feeding behavior is wanting, although molecular phylogenies indicate that it evolved independently in the two lineages.4 We describe a new extinct representative of the killer whale ecomorph, Rododelphis stamatiadisi, based on a partial skeleton from the Pleistocene of Rhodes (Greece). Five otoliths of the bathypelagic blue whiting Micromesistius poutassou are associated with the holotype, providing unexpected evidence of its last meal. The evolutionary relationships of R. stamatiadisi and the convergent evolution of killer whale-like features were explored through a broad-ranging phylogenetic analysis that recovered R. stamatiadisi as the closest relative of P. crassidens and O. orca as the only living representative of a once diverse clade. Within the clade of Orca and kin, key features implicated in extant killer whale feeding, such as body size, tooth size, and tooth count, evolved in a stepwise manner. The tooth wear in Rododelphis and an extinct species of Orcinus (O. citoniensis) are consistent with a fish-based diet, supporting an exaptative Pleistocene origin for marine mammal hunting in both lineages. If correct, predation by the ancestors of Pseudorca and Orca did not play a significant role in the evolution of baleen whale gigantism. VIDEO ABSTRACT.

The tempo of cetacean cranial evolution.

The evolution of cetaceans (whales and dolphins) represents one of the most extreme adaptive transitions known, from terrestrial mammals to a highly specialized aquatic radiation that includes the largest animals alive today. Many anatomical shifts in this transition involve the feeding, respiratory, and sensory structures of the cranium, which we quantified with a high-density, three-dimensional geometric morphometric analysis of 201 living and extinct cetacean species spanning the entirety of their ∼50-million-year evolutionary history. Our analyses demonstrate that cetacean suborders occupy distinct areas of cranial morphospace, with extinct, transitional taxa bridging the gap between archaeocetes (stem whales) and modern mysticetes (baleen whales) and odontocetes (toothed whales). This diversity was obtained through three key periods of rapid evolution: first, the initial evolution of archaeocetes in the early to mid-Eocene produced the highest evolutionary rates seen in cetaceans, concentrated in the maxilla, frontal, premaxilla, and nasal; second, the late Eocene divergence of the mysticetes and odontocetes drives a second peak in rates, with high rates and disparity sustained through the Oligocene; and third, the diversification of odontocetes, particularly sperm whales, in the Miocene (∼18-10 Mya) propels a final peak in the tempo of cetacean morphological evolution. Archaeocetes show the fastest evolutionary rates but the lowest disparity. Odontocetes exhibit the highest disparity, while mysticetes evolve at the slowest pace, particularly in the Neogene. Diet and echolocation have the strongest influence on cranial morphology, with habitat, size, dentition, and feeding method also significant factors impacting shape, disparity, and the pace of cetacean cranial evolution.

A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea.

BACKGROUND: Cetacea (dolphins, porpoises, and whales) is a clade of aquatic species that includes the most massive, deepest diving, and largest brained mammals. Understanding the temporal pattern of diversification in the group as well as the evolution of cetacean anatomy and behavior requires a robust and well-resolved phylogenetic hypothesis. Although a large body of molecular data has accumulated over the past 20 years, DNA sequences of cetaceans have not been directly integrated with the rich, cetacean fossil record to reconcile discrepancies among molecular and morphological characters. RESULTS: We combined new nuclear DNA sequences, including segments of six genes (~2800 basepairs) from the functionally extinct Yangtze River dolphin, with an expanded morphological matrix and published genomic data. Diverse analyses of these data resolved the relationships of 74 taxa that represent all extant families and 11 extinct families of Cetacea. The resulting supermatrix (61,155 characters) and its sub-partitions were analyzed using parsimony methods. Bayesian and maximum likelihood (ML) searches were conducted on the molecular partition, and a molecular scaffold obtained from these searches was used to constrain a parsimony search of the morphological partition. Based on analysis of the supermatrix and model-based analyses of the molecular partition, we found overwhelming support for 15 extant clades. When extinct taxa are included, we recovered trees that are significantly correlated with the fossil record. These trees were used to reconstruct the timing of cetacean diversification and the evolution of characters shared by "river dolphins," a non-monophyletic set of species according to all of our phylogenetic analyses. CONCLUSIONS: The parsimony analysis of the supermatrix and the analysis of morphology constrained to fit the ML/Bayesian molecular tree yielded broadly congruent phylogenetic hypotheses. In trees from both analyses, all Oligocene taxa included in our study fell outside crown Mysticeti and crown Odontoceti, suggesting that these two clades radiated in the late Oligocene or later, contra some recent molecular clock studies. Our trees also imply that many character states shared by river dolphins evolved in their oceanic ancestors, contradicting the hypothesis that these characters are convergent adaptations to fluvial habitats.

Convergent Evolution of Swimming Adaptations in Modern Whales Revealed by a Large Macrophagous Dolphin from the Oligocene of South Carolina.

Modern whales and dolphins are superbly adapted for marine life, with tail flukes being a key innovation shared by all extant species. Some dolphins can exceed speeds of 50 km/h, a feat accomplished by thrusting the flukes while adjusting attack angle with their flippers [1]. These movements are driven by robust axial musculature anchored to a relatively rigid torso consisting of numerous short vertebrae, and controlled by hydrofoil-like flippers [2-7]. Eocene skeletons of whales illustrate the transition from semiaquatic to aquatic locomotion, including development of a fusiform body and reduction of hindlimbs [8-11], but the rarity of Oligocene whale skeletons [12, 13] has hampered efforts to understand the evolution of fluke-powered, but forelimb-controlled, locomotion. We report a nearly complete skeleton of the extinct large dolphin Ankylorhiza tiedemani comb. n. from the Oligocene of South Carolina, previously known only from a partial rostrum. Its forelimb is intermediate in morphology between stem cetaceans and extant taxa, whereas its axial skeleton displays incipient rigidity at the base of the tail with a flexible lumbar region. The position of Ankylorhiza near the base of the odontocete radiation implies that several postcranial specializations of extant cetaceans, including a shortened humerus, narrow peduncle, and loss of radial tuberosity, evolved convergently in odontocetes and mysticetes. Craniodental morphology, tooth wear, torso vertebral morphology, and body size all suggest that Ankylorhiza was a macrophagous predator that could swim relatively fast, indicating that it was one of the few extinct cetaceans to occupy a niche similar to that of killer whales.

New records of the archaic dolphin Agorophius (Mammalia: Cetacea) from the upper Oligocene Chandler Bridge Formation of South Carolina, USA.

The stem odontocete Agorophius pygmaeus (Ashley Formation, lower Oligocene, South Carolina; 29.0-26.57 Ma) has been a critical point of comparison for studies of early neocete evolution owing to its early discovery as well as its transitional anatomy relative to archaeocete whales and modern odontocetes. Some time during the late nineteenth century the holotype skull went missing and has never been relocated; supplementary reference specimens have since been recently referred to the species from the Ashley Formation and the overlying Chandler Bridge Formation (upper Oligocene; 24.7-23.5). New crania referable to Agorophius sp. are identifiable to the genus based on several features of the intertemporal region. Furthermore, all published specimens from the Chandler Bridge Formation consistently share larger absolute size and a proportionally shorter exposure of the parietal in the skull roof than specimens from the Ashley Formation (including the holotype). Furthermore, these specimens include well-preserved ethmoid labyrinths and cribriform plates, indicating that Agorophius primitively retained a strong olfactory sense. These new crania suggest that at least two species of Agorophius are present in the Oligocene of South Carolina, revealing a somewhat more complicated taxonomic perspective.

Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti).

Odontocete (echolocating whale) skulls exhibit extreme posterior displacement and overlapping of facial bones, here referred to as retrograde cranial telescoping. To examine retrograde cranial telescoping across 40 million years of whale evolution, we collected 3D scans of whale skulls spanning odontocete evolution. We used a sliding semilandmark morphometric approach with Procrustes superimposition and PCA to capture and describe the morphological variation present in the facial region, followed by Ancestral Character State Reconstruction (ACSR) and evolutionary model fitting on significant components to determine how retrograde cranial telescoping evolved. The first PC score explains the majority of variation associated with telescoping and reflects the posterior migration of the external nares and premaxilla alongside expansion of the maxilla and frontal. The earliest diverging fossil odontocetes were found to exhibit a lesser degree of cranial telescoping than later diverging but contemporary whale taxa. Major shifts in PC scores and centroid size are identified at the base of Odontoceti, and early burst and punctuated equilibrium models best fit the evolution of retrograde telescoping. This indicates that the Oligocene was a period of unusually high diversity and evolution in whale skull morphology, with little subsequent evolution in telescoping.

New records of the dolphin Albertocetus meffordorum (Odontoceti: Xenorophidae) from the lower Oligocene of South Carolina: Encephalization, sensory anatomy, postcranial morphology, and ontogeny of early odontocetes.

We report five new specimens of xenorophid dolphins from North and South Carolina. Four of the specimens represent the xenorophid Albertocetus meffordorum, previously only known from the holotype skull. The other is a fragmentary petrosal from the upper Oligocene Belgrade Formation that we refer to Echovenator sp, indicating at least two xenorophids from that unit. Two of the Albertocetus meffordorum specimens are from the lower Oligocene Ashley Formation: 1) a partial skeleton with neurocranium, fragmentary mandible, ribs, vertebrae, and chevrons, and 2) an isolated braincase. The partial vertebral column indicates that Albertocetus retained the ancestral morphology and locomotory capabilities of basilosaurid archaeocetes, toothed mysticetes, and physeteroids, and caudal vertebrae that are as wide as tall suggest that the caudal peduncle, which occurs in all extant Cetacea, was either wide or lacking. CT data from the isolated braincase were used to generate a digital endocast of the cranial cavity. The estimated EQ of this specimen is relatively high for an Oligocene odontocete, and other aspects of the brain, such as its anteroposterior length and relative size of the temporal lobe, are intermediate in morphology between those of extant cetaceans and terrestrial artiodactyls. Ethmoturbinals are also preserved, and are similar in morphology and number to those described for the Miocene odontocete Squalodon. These fossils extend the temporal range of Albertocetus meffordorum into the early Oligocene, its geographic range into South Carolina, and expand our paleobiological understanding of the Xenorophidae.

The Origin of Filter Feeding in Whales.

As the largest known vertebrates of all time, mysticetes depend on keratinous sieves called baleen to capture enough small prey to sustain their enormous size [1]. The origins of baleen are controversial: one hypothesis suggests that teeth were lost during a suction-feeding stage of mysticete evolution and that baleen evolved thereafter [2-4], whereas another suggests that baleen evolved before teeth were lost [5]. Here we report a new species of toothed mysticete, Coronodon havensteini, from the Oligocene of South Carolina that is transitional between raptorial archaeocete whales and modern mysticetes. Although the morphology and wear on its anterior teeth indicate that it captured large prey, its broad, imbricated, multi-cusped lower molars frame narrow slots that were likely used for filter feeding. Coronodon havensteini is a basal, if not the most basal, mysticete, and our analysis suggests that it is representative of an initial stage of mysticete evolution in which teeth were functional analogs to baleen. In later lineages, the diastema between teeth increased-in some cases, markedly so [6]-and may mark a stage at which the balance of the oral fissure shifted from mostly teeth to mostly baleen. When placed in a phylogenetic context, our new taxon indicates that filter feeding was preceded by raptorial feeding and that suction feeding evolved separately within a clade removed from modern baleen whales.

The Origin of High-Frequency Hearing in Whales.

Odontocetes (toothed whales) rely upon echoes of their own vocalizations to navigate and find prey underwater [1]. This sensory adaptation, known as echolocation, operates most effectively when using high frequencies, and odontocetes are rivaled only by bats in their ability to perceive ultrasonic sound greater than 100 kHz [2]. Although features indicative of ultrasonic hearing are present in the oldest known odontocetes [3], the significance of this finding is limited by the methods employed and taxa sampled. In this report, we describe a new xenorophid whale (Echovenator sandersi, gen. et sp. nov.) from the Oligocene of South Carolina that, as a member of the most basal clade of odontocetes, sheds considerable light on the evolution of ultrasonic hearing. By placing high-resolution CT data from Echovenator sandersi, 2 hippos, and 23 fossil and extant whales in a phylogenetic context, we conclude that ultrasonic hearing, albeit in a less specialized form, evolved at the base of the odontocete radiation. Contrary to the hypothesis that odontocetes evolved from low-frequency specialists [4], we find evidence that stem cetaceans, the archaeocetes, were more sensitive to high-frequency sound than their terrestrial ancestors. This indicates that selection for high-frequency hearing predates the emergence of Odontoceti and the evolution of echolocation.

The evolutionary history of cetacean brain and body size.

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.