Early cetaceans evolved from terrestrial quadrupeds to obligate swimmers, a change that is traditionally studied by functional analysis of the postcranial skeleton. Here we assess the evolution of cetacean locomotor behaviour from an independent perspective by looking at the semicircular canal system, one of the main sense organs involved in neural control of locomotion. Extant cetaceans are found to be unique in that their canal arc size, corrected for body mass, is approximately three times smaller than in other mammals. This reduces the sensitivity of the canal system, most plausibly to match the fast body rotations that characterize cetacean behaviour. Eocene fossils show that the new sensory regime, incompatible with terrestrial competence, developed quickly and early in cetacean evolution, as soon as the taxa are associated with marine environments. Dedicated agile swimming of cetaceans thus appeared to have originated as a rapid and fundamental shift in locomotion rather than as the gradual transition suggested by postcranial evidence. We hypothesize that the unparalleled modification of the semicircular canal system represented a key 'point of no return' event in early cetacean evolution, leading to full independence from life on land.

Although the first ten million years of whale evolution are documented by a remarkable series of fossil skeletons, the link to the ancestor of cetaceans has been missing. It was known that whales are related to even-toed ungulates (artiodactyls), but until now no artiodactyls were morphologically close to early whales. Here we show that the Eocene south Asian raoellid artiodactyls are the sister group to whales. The raoellid Indohyus is similar to whales, and unlike other artiodactyls, in the structure of its ears and premolars, in the density of its limb bones and in the stable-oxygen-isotope composition of its teeth. We also show that a major dietary change occurred during the transition from artiodactyls to whales and that raoellids were aquatic waders. This indicates that aquatic life in this lineage occurred before the origin of the order Cetacea.

Modern members of the mammalian order Cetacea (whales, dolphins and porpoises) are obligate aquatic swimmers that are highly distinctive in morphology, lacking hair and hind limbs, and having flippers, flukes, and a streamlined body. Eocene fossils document much of cetaceans' land-to-water transition, but, until now, the most primitive representative for which a skeleton was known was clearly amphibious and lived in coastal environments. Here we report on the skeletons of two early Eocene pakicetid cetaceans, the fox-sized Ichthyolestes pinfoldi, and the wolf-sized Pakicetus attocki. Their skeletons also elucidate the relationships of cetaceans to other mammals. Morphological cladistic analyses have shown cetaceans to be most closely related to one or more mesonychians, a group of extinct, archaic ungulates, but molecular analyses have indicated that they are the sister group to hippopotamids. Our cladistic analysis indicates that cetaceans are more closely related to artiodactyls than to any mesonychian. Cetaceans are not the sister group to (any) mesonychians, nor to hippopotamids. Our analysis stops short of identifying any particular artiodactyl family as the cetacean sister group and supports monophyly of artiodactyls.

During development and evolution, the morphology of ectodermal organs can be modulated so that an organism can adapt to different environments. We have proposed that morphoregulation can be achieved by simply tilting the balance of molecular activity. We test the principles by analyzing the effects of partial downregulation of Bmp signaling in oral and dental epithelia of the keratin 14-Noggin transgenic mouse. We observed a wide spectrum of tooth phenotypes. The dental formula changed from 1.0.0.3/1.0.0.3 to 1.0.0.2(1)/1.0.0.0. All mandibular and M3 maxillary molars were selectively lost because of the developmental block at the early bud stage. First and second maxillary molars were reduced in size, exhibited altered crown patterns, and failed to form multiple roots. In these mice, incisors were not transformed into molars. Histogenesis and differentiation of ameloblasts and odontoblasts in molars and incisors were abnormal. Lack of enamel caused misocclusion of incisors, leading to deformation and enlargement in size. Therefore, subtle differences in the level, distribution, and timing of signaling molecules can have major morphoregulatory consequences. Modulation of Bmp signaling exemplifies morphoregulation hypothesis: simple alteration of key signaling pathways can be used to transform a prototypical conical-shaped tooth into one with complex morphology. The involvement of related pathways and the implication of morphoregulation in tooth evolution are discussed.

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.

Among mammals, modern cetaceans (whales, dolphins, and porpoises) are unusual in the absence of hind limbs. However, cetacean embryos do initiate hind-limb bud development. In dolphins, the bud arrests and degenerates around the fifth gestational week. Initial limb outgrowth in amniotes is maintained by two signaling centers, the apical ectodermal ridge (AER) and the zone of polarizing activity (ZPA). Our data indicate that the cetacean hind-limb bud forms an AER and that this structure expresses Fgf8 initially, but that neither the AER nor Fgf8 expression is maintained. Moreover, Sonic hedgehog (Shh), which mediates the signaling activity of the ZPA, is absent from the dolphin hind-limb bud. We find that failure to establish a ZPA is associated with the absence of Hand2, an upstream regulator of Shh. Interpreting our results in the context of both the cetacean fossil record and the known functions of Shh suggests that reduction of Shh expression may have occurred Ϸ41 million years ago and led to the loss of distal limb elements. The total loss of Shh expression may account for the further loss of hind-limb elements that occurred near the origin of the modern suborders of cetaceans Ϸ34 million years ago. Integration of paleontological and developmental data suggests that hind-limb size was reduced by gradually operating microevolutionary changes. Long after locomotor function was totally lost, modulation of developmental control genes eliminated most of the hind-limb skeleton. Hence, macroevolutionary changes in gene expression did not drive the initial reduction in hind-limb size.cetacea ͉ delphinidae ͉ evo-devo ͉ limb development ͉ whale evolution

The whale ear, initially designed for hearing in air, became adapted for hearing underwater in less than ten million years of evolution. This study describes the evolution of underwater hearing in cetaceans, focusing on changes in sound transmission mechanisms. Measurements were made on 60 fossils of whole or partial skulls, isolated tympanics, middle ear ossicles, and mandibles from all six archaeocete families. Fossil data were compared with data on two families of modern mysticete whales and nine families of modern odontocete cetaceans, as well as five families of noncetacean mammals. Results show that the outer ear pinna and external auditory meatus were functionally replaced by the mandible and the mandibular fat pad, which posteriorly contacts the tympanic plate, the lateral wall of the bulla. Changes in the ear include thickening of the tympanic bulla medially, isolation of the tympanoperiotic complex by means of air sinuses, functional replacement of the tympanic membrane by a bony plate, and changes in ossicle shapes and orientation. Pakicetids, the earliest archaeocetes, had a land mammal ear for hearing in air, and used bone conduction underwater, aided by the heavy tympanic bulla. Remingtonocetids and protocetids were the first to display a genuine underwater ear where sound reached the inner ear through the mandibular fat pad, the tympanic plate, and the middle ear ossicles. Basilosaurids and dorudontids showed further aquatic adaptations of the ossicular chain and the acoustic isolation of the ear complex from the skull. The land mammal ear and the generalized modern whale ear are evolutionarily stable configurations, two ends of a process where the cetacean mandible might have been a keystone character.

IntroductionWhile olfaction is one of the most important senses in most terrestrial mammals, it is absent in modern toothed whales (Odontoceti, Cetacea). Furthermore, behavioral evidence suggests that gustation is very limited. In contrast, their aquatic sistergroup, baleen whales (Mysticeti) retain small but functional olfactory organs, and nothing is known about their gustation. It is difficult to investigate mysticete chemosensory abilities because experiments in a controlled setting are impossible.ResultsHere, we use the functional regionalization of the olfactory bulb (OB) to identify the loss of specific olfactory functions in mysticetes. We provide the whole-genome sequence of a mysticete and show that mysticetes lack the dorsal domain of the OB, an area known to induce innate avoidance behavior against odors of predators and spoiled foods. Genomic and fossil data suggest that mysticetes lost the dorsal domain of the OB before the Odontoceti-Mysticeti split. Furthermore, we found that all modern cetaceans are revealed to have lost the functional taste receptors.ConclusionThese results strongly indicate that profound changes in the chemosensory capabilities had occurred in the cetacean lineage during the period when ancestral whales migrated from land to water.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-014-0002-z) contains supplementary material, which is available to authorized users.