Cetacean Evolutionary History
Pakicetus, one of the earliest cetaceans (Gingerich et al., 1983) was a rather terrestrial animal when compared with most other cetaceans (see Fig. 2A; Thewissen et al., 2001). The limbs and vertebral column show very little change in morphology, but they do have some histological changes that indicate they walked around in shallow water (Madar, 1998). The skull and dentition do, however, show changes indicating activity in the water. The anterior end of the rostrum is elongate, which arranges the incisors in a line with the cheek teeth, rather than in an arc across the front of the snout as in most mammals. This arrangement also has the effect of placing the external nares posterior to the tip of the rostrum, because the premaxilla is elongated anterior to the external nares.
Figure 2. Skeletal reconstructions of early representatives of each marine mammal clade. A:Pakicetus (from Thewissen et al., 2001). B:Pezosiren (from Domning, 2001a). C:Paleoparadoxia (from Domning, 2002b). D:Enaliarctos (from Berta et al., 1989). Drawings are not to scale, but have been shown at the same neck and trunk length for comparative purposes.
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Comparison of the wear facets on the teeth of Pakicetus and all other archaeocetes indicates that they chewed in a very different manner than terrestrial mammals of the time (O'Leary and Uhen, 1999). The eyes are positioned rather high on the lateral sides of the skull. The ectotympanic of Pakicetus is large and inflated into the tympanic bulla that is characteristic of all cetaceans. The dense bone and large size of the bulla is interpreted to be an adaptation for hearing sounds underwater rather than in the air. Fossils of Pakicetus are found in fluviatile (river) deposits, and studies of the oxygen isotopes incorporated into the enamel of the teeth indicate that Pakicetus ingested freshwater (Thewissen et al., 1996).
Slightly younger cetaceans such as the early protocetid Rodhocetus (Gingerich et al., 1994b, 2001) show a further development of the adaptations seen in pakicetids, with more changes apparent in the appendicular and axial skeletons. In Rodhocetus, the teeth have a similar arrangement as in Pakicetus, but the cusp patterns are becoming more simplified on the cheek teeth. Analysis of the oxygen isotopes incorporated into the enamel of the teeth indicate that Indocetus, a close relative of Rodhocetus, ingested only sea water, to the exclusion of fresh water (Thewissen et al., 1996). The nares are relatively farther from the anterior tip of the rostrum. The bulla is more inflated in Rodhocetus and less well connected to the skull than in Pakicetus. This finding has the effect of increasing the ability to hear directionally underwater. Also, protocetids and all later cetaceans have a greatly enlarged mandibular canal and mandibular foramen. In modern odontocetes, this space is filled with a mandibular fat body that connects back to the bulla, forming a secondary path for sound to travel to the middle ear as opposed to the external auditory meatus. This finding also increased the ability to hear directionally under water. While Rodhocetus still has hind limbs that function on land, they are reduced in size when compared with terrestrial mammals (Gingerich et al., 1994b, 2001). Rodhocetus also has sacral vertebrae that articulate with the pelves and each other, but they are not fused to one another (Gingerich et al., 1994b).
Slightly younger protocetids such as Protocetus or Natchitochia have a single sacral vertebra, or no sacral vertebrae that attached to the pelves (Georgiacetus; Uhen, 1998a). An animal such as Georgiacetus could not use the hind limbs for locomotion on land, because they lack a bony connection to the axial skeleton, but could have used their hind limbs as propulsive surfaces in the water, moved by flexion and extension of the vertebral column.
Basilosaurid archaeocetes such as Dorudon and Zygorhiza have teeth that are significantly modified from the earliest archaeocetes. They have lost virtually all of their bucco-lingual dimensionality and have become flat blades in the plane of the jaw. Basilosaurids have also developed accessory denticles on the cheek teeth that were lacking in earlier archaeocetes, perhaps for better gripping of prey items while undergoing oral processing (Uhen, 1998b). The auditory region of basilosaurids is further modified by the expansion of bony sinuses around the auditory bulla, which is even further detached from the basicranium. In modern cetaceans, these sinuses are filled with air to help acoustically isolate the ear from the rest of the skull (Uhen, 1998b).
The postcranial skeletons of basilosaurids are also significantly modified for a fully aquatic existence (Uhen, 1998b). The forelimbs have broad scapulae characteristic of modern cetaceans, along with very restricted motion at the elbow and wrists, indicating an inability to draw the forelimbs under the body for terrestrial locomotion. The vertebrae of the trunk have become very uniform in size and shape, which is interpreted as a response to the lack of differential loading of the vertebral column at the limbs. The number of vertebrae has also increased, lengthening the body, and increasing the number of attachment sites for trunk muscles that drive the tail in modern cetaceans. Basilosaurids lack sacral vertebrae, and the caudal vertebrae have become highly modified posteriorly (flat and rather square in shape), which indicates the presence of soft tissue tail flukes, even though they have never been preserved in a fossil cetacean (Uhen, 2004). The hind limbs are so reduced that they are not thought to have had any function in locomotion (Gingerich et al., 1990; Uhen and Gingerich, 2001).
Basilosaurids gave rise to both the odontocetes and mysticetes. In both groups, the external nares continue to migrate posteriorly to a point on top of the skull between or behind the orbits. Odontocetes also reorganize the bones of the face such that the primitively anterior bones are layered on top of those that were more posterior in archaeocetes. The origin of echolocation in odontocetes is indicated by the presence of facial structures involved in the production of outgoing sound such as the premaxillary sac fossae, and in the modification of the inner ear for the perception of high frequency sound. In mysticetes more posterior bones of the occipital region are thrust forward on the skull. Also, while early mysticetes have teeth that were probably used in filter feeding (e.g., Llanocetus, Mitchell, 1989), these teeth become reduced in size (e.g., Aetiocetus, Emlong, 1966) and eventually are lost (e.g., Eomysticetus, Sanders and Barnes, 2002). The presence of baleen can be inferred from the presence of vascular grooves in the palate, which in modern mysticetes feed the gums that support the baleen.
Sirenian Evolutionary History
The earliest sirenians (prorastomids) were long-bodied quadrupeds with limbs that functioned for terrestrial locomotion (see Fig. 2B; Domning and Gingerich, 1994; Domning, 2001a), but are found exclusively in marine rocks. Savage et al. (1994) suggest that the prorastomids were fluviatile or estuarine, to marginal marine animals with diets similar to the modern sea cow, Trichechus. This conclusion is in part based on the lack of a great deal of deflection of the rostrum and the narrowness of the snout, which suggests a more selective browser than the seagrass grazers such as the modern Dugong (Savage et al., 1994; Domning, 2001c).
Prorastomid ribs are pachyosteosclerotic (both dense and swollen in diameter) (Domning and Buffrénil, 1991), which is often interpreted as a form of ballast to weigh down the body while in water. Digestion of plant material produces a great deal of buoyant gas that would tend to make the body float, thus increased ballast would help maintain neutral or negative buoyancy, and thus save energy while staying close to the bottom. The size and shape of vertebral processes and joint surfaces shows that Pezosiren, one of the most completely known early sirenians, was fully capable of terrestrial locomotion. Other features, such as the retracted nares, lack of paranasal air sinuses, and pachyosteosclerotic ribs indicate that it spent most of its time in the water (Domning, 2001a).
Computed tomography (CT) scans of the skull of Protosiren show that it had small olfactory bulbs and a small optic tract, indicating a decreased use of smell and vision, respectively (Gingerich et al., 1994a). All sirenians have a down-turned snout that is used for feeding on plants attached to the sea floor, particularly the rhizomes. MacFadden et al. (2004) show that protosirenids were almost exclusively seagrass feeders based on the oxygen isotopic composition of their teeth. Differentiation of sirenian diets into seagrass feeders, floating vegetation feeders, and marine algae feeders occurred much later in their evolutionary history, during the Oligocene and Miocene.
By the latest Eocene, sirenians had reduced their hind limbs to the point where they were fully aquatic (Domning, 2001b). It is unclear when in their evolutionary history the tail flukes developed. Modern trichechids have broad, round flukes, whereas dugongs have more triangular flukes like those of modern cetaceans. Sirenians have been restricted to tropical and subtropical waters because they feed on angiospermous plants that are themselves secondarily aquatic and mostly tropical or subtropical. The only exception to this general rule is hydrodamalines, which lived in the cold waters of the North Pacific, and are thought to have fed on marine algae.
Desmostylian Evolutionary History
Desmostylians are most characteristically distinguished from other mammals by their strange cheek teeth that possess columns of thick enamel surrounding a dentine core (Domning, 2002a). Desmostylians also have procumbent incisors and canines with a long diastema between the anterior teeth and the cheek teeth.
Desmostylian postcrania have puzzled researchers since their earliest discovery. Some have reconstructed them in postures like modern sea lions, frogs, and hippos (see Fig. 2C; Domning, 2001b, 2002b). Desmostylian remains are found exclusively in marginal marine deposits of the North Pacific, indicating a preference for subtropical to cold water habitats. Of interest, the skeletons of desmostylians have virtually no adaptations to an aquatic environment. The interpretation of their life habit as amphibious is based almost entirely on their being found exclusively in marginal marine rocks. One study of the carbon and oxygen isotopic composition of the teeth of the Miocene genus Desmostylus concluded that it had a diet that consisted of seagrasses, with a good portion of freshwater and estuarine aquatic vegetation, not unlike the diet of modern Trichechus (Clementz et al., 2003).
Pinniped Evolutionary History
The earliest well-known pinniped, or pinnipedimorph as they are sometimes called, is Enaliarctos, from the late Oligocene of Oregon and California (see Fig. 2D; Berta et al., 1989; Berta, 1991). Enaliarctos was originally known only from partial skulls and teeth (Mitchell and Tedford, 1973) and was initially interpreted as an otarioid pinniped. Subsequent phylogenetic analyses (Wyss, 1988; Berta, 1991) demonstrated that Enaliarctos represented the sister taxon to all other pinnipeds.
The first skulls and teeth described for Enaliarctos led Mitchell and Tedford (1973) to conclude that Enaliarctos was indeed a pinniped, noting that: “In the dentition of Enaliarctos we see an intermediate stage in the transformation of the generalized fissiped dentition from a multipurpose structure to a specialized device for capturing fish and nektonic invertebrates.” Berta et al. (1989) noted that both the appendicular and axial skeleton of Enaliarctos show several features indicating a pelagic existence. The lumbar vertebrae have long transverse processes and large metapophyses where hypaxial and epaxial muscles attach, resulting in a wide range of vertical and lateral movements (Berta et al., 1989). Enaliarctos also has the fore- and hindlimbs modified into powerfully muscled flippers (Berta et al., 1989). The morphology of the axial and appendicular skeleton taken together indicate that Enaliarctos swam with both the axial skeleton and all four limbs (Berta et al., 1989).
Interestingly, the proximal sister taxon to pinnipeds (Pinnipedimorpha) is thought to be Kolponomos, a semiaquatic amphicynodontid ursoid, which is known from the early Miocene marginal marine deposits of Oregon and Washington (Tedford et al., 1994). Kolponomos has crushing cheek teeth that are thought to have been used for a diet of hard-shelled invertebrates. It also has anteriorly directed eyes and a down-turned snout that would help it to selectively feed on epifaunal invertebrates (Tedford et al., 1994). A few vertebrae and foot bones have been attributed to Kolponomos that suggest it was not a strong swimmer (Tedford et al., 1994).