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Keywords:

  • cetacea;
  • sirenia;
  • pinnipedia;
  • carnirora;
  • desmostylia;
  • feeding ecology;
  • aquatic adaptation

Abstract

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

The fossil record demonstrates that mammals re-entered the marine realm on at least seven separate occasions. Five of these clades are still extant, whereas two are extinct. This review presents a brief introduction to the phylogeny of each group of marine mammals, based on the latest studies using both morphological and molecular data. Evolutionary highlights are presented, focusing on changes affecting the sensory systems, locomotion, breathing, feeding, and reproduction in Cetacea, Sirenia, Desmostylia, and Pinnipedia. Aquatic adaptations are specifically cited, supported by data from morphological and geochemical studies. For example, analysis of oxygen isotopes incorporated into fossil tooth enamel indicates whether these mammals foraged in (and, therefore, ingested) fresh water or sea water. Comparisons between groups are made to see if there are any common patterns, particularly relating to adaptations to aquatic life. Results show that aquatic characteristics evolved in mosaic patterns and that different morphological solutions to aquatic conditions were achieved separately in each of these groups. Changes in the axial and appendicular skeleton assist with locomotion for aquatic foraging. Nostril and eye placement modifications accommodate wading versus underwater foraging needs. All groups exhibit aquatic adaptations directly related to feeding, particularly changes in the dentition and rostrum. The earliest representatives of these clades all show morphological features that indicate they were feeding while in the water, suggesting that feeding ecology is a key factor in the evolution of marine mammals. Anat Rec, 290:514–522, 2007. © 2007 Wiley-Liss, Inc.

A recurrent theme in tetrapod evolution is a return to an aquatic habitat. Whereas amphibians never quite parted with the water, all other tetrapod groups (reptiles, birds, and mammals) have several representatives that have returned to the water for at least an amphibious lifestyle of some degree, if not a fully aquatic existence. Mammals in particular have returned to the water in at least seven separate lineages (Cetacea, Sirenia, Desmostylia, Pinnipedia, Ursus maritimus [polar bear], Enhydra lutris [sea otter], and Thalassocnusspp. [aquatic sloths]). Some of these lineages have retained most of their terrestrial form while spending a great deal of time in the water, whereas others have changed their morphology dramatically and spend almost all, if not all, of their time in the water.

Before exploring how the anatomical changes for life in water came about, one must know how marine mammals are related to one another, and particularly to their terrestrial relatives. A brief introduction to the phylogeny of each group of marine mammals is presented here, based on the latest studies using both morphological and molecular data.

CETACEAN PHYLOGENY

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

The relationships of cetaceans to terrestrial mammals and other marine mammals was a great mystery for many natural historians of the past. At times, cetaceans and sirenians were grouped together because of some of their superficially similar anatomical structure such as loss of hind limbs, modification of the forelimbs into flippers, and fluked tails. Even as recently as the early twentieth century, George Gaylord Simpson (1945) placed Cetacea in a Cohort Mutica by themselves, because he could not confidently relate them to other mammals. Since that time, a great deal has been learned about the relationships of whales to other mammals, and to each other.

For a time, paleontologists supported a hypothesis put forth by Van Valen (1966) that cetaceans were most closely related to a group of fossil ungulates known as mesonychians, mainly based on shared characteristics of their teeth (O'Leary and Geisler, 1999; Geisler, 2001), and that the closest living relatives of cetaceans were the artiodactyls. At the same time, molecular evidence was mounting that, not only were artiodactyls the closest living sister taxon to whales, but whales were derived from well within the artiodactyl clade, and that whales were the sister taxon to hippopotamuses. These two divergent opinions merged in 2001 when separate discoveries of the feet and ankles of early whales (Gingerich et al., 2001; Thewissen et al., 2001) demonstrated the artiodactyl nature of the early cetacean foot. Subsequent phylogenetic analyses of the morphological and the molecular data supported the hypothesis that whales are most closely related to Hippopotamidae (Geisler and Uhen, 2003, 2005).

Within Cetacea, relationships among families are still often hotly debated and are being studied with both morphological (Geisler and Sanders, 2003) and genetic (Arnason et al., 2004) techniques. Most agree that Physeteridae (sperm whales) and Ziphiidae (beaked whales) are among the earliest of living groups to branch off within the odontocete clade after the split of Odontoceti and Mysticeti, which appears to have occurred at or perhaps just before the Eocene/Oligocene boundary (Fordyce, 2002). Much of the debate about relationships within the Odontoceti center on the placement of the various groups of “river dolphins” (Iniidae, Lipotidae, Platanistidae, and Pontoporiidae). See Geisler and Sanders (2003) and Cassens et al. (2000) for contrasting approaches (morphological and molecular) and results. Within Mysticeti, most phylogenetic questions are found among the fossil taxa, because there are so few living genera, and they all tend to form well-resolved clades (Deméré et al., 2005).

SIRENIAN AND DESMOSTYLIAN PHYLOGENY

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

Sirenians are part of a larger group of mammals known as the Tethytheria, named after the Tethys Sea, near which they are considered to have evolved. Tethytheria includes Sirenia, Proboscidea, and Desmostylia. The interrelationships of these three taxa (as well as other groups like Anthracobunia and Embrithopoda) have been reconstructed in almost all possible combinations (Gheerbrant et al., 2005a). One of the better-supported phylogenetic analyses (Gheerbrant et al., 2005a) has Sirenia and Proboscidea as sister taxa, with Desmostylia more distantly related.

Desmostylians represent an extinct order of semiaquatic herbivorous mammals, known only from the Oligocene and Miocene marginal marine deposits of the north Pacific (Domning et al., 1986). For such a small group of mammals (six currently recognized genera), there has been a great deal of debate about their lifestyle and their relationship to other mammals. The relationships among Desmostylia, Sirenia, and Proboscidea indicate that either the common ancestor of the three groups was semiaquatic, and the Proboscidea secondarily became fully terrestrial, or that the Desmostylia and Sirenia each invaded the aquatic environment separately. Currently, the morphological and phylogenetic data are not clear enough to fully resolve this issue, although the style of aquatic locomotion in Desmostylia and Sirenia are very different, suggesting that each may have invaded the aquatic habitat independently (Domning, 2001b, 2002a; Gingerich, 2005a).

MARINE CARNIVORE PHYLOGENY

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

Two members of the Order Carnivora that are semiaquatic, the polar bear and the sea otter, are clearly recently derived from terrestrial clades (Ursidae and Mustelidae respectively; Berta et al., 2006). The Pinnipedia, or as the somewhat more inclusive clade is often named, Pinnipedimorpha, are clearly arctoid carnivores, most likely derived from basal ursids, although there is some debate about which arctoid carnivore group is the sister taxon to pinnipeds (see Berta et al., 2006, and references therein). Some pinniped workers support a diphyletic origin for pinnipeds, with phocids derived from basal Mustellidae, and otarioids derived from basal ursids (e.g., Muizon, 1982). This hypothesis has not yet been supported by rigorous cladistic analysis. Both morphological (Berta and Wyss, 1994) and molecular (Flynn et al., 2005) analyses support a monophyletic origin of pinnipeds from basal ursids.

Recent molecular studies have generally supported the sister taxon relationship of Ursida with pinnipeds, but have also included some analyses that support a closer relationship between mustelids and pinnipeds (Davis et al., 2004). Despite this lack of a clear sister taxon for pinnipeds within Arctoidea, these analyses support an otariid-odobenid clade, which is a sister to phocids within a monophyletic Pinnipedia (Davis et al., 2004). Devinophoca, a recently described, early Miocene phocid from eastern Europe displays a mix of plesiomorphic and derived phocid characters (Koretsky and Holec, 2002). These authors place Devinophoca at the base of the phocid clade and suggest that it has some characters in common with Enaliarctos and others with mustelids (Koretsky and Holec, 2002), but they do not place Devinophoca or other phocids into a phylogenetic analysis of potential sister taxa and, thus, do not address the question of pinniped monophyly vs. pinniped diphyly.

WHY DID MARINE MAMMALS GO BACK TO THE SEA?

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

This is probably the most difficult question for a marine mammalogist, and the one most often asked. Those of us who study the history of marine mammals can describe the circumstances, the evolutionary pathways, the relationships, and even some of the behaviors of these early representatives of the clades of marine mammals, but we have difficulty with the question of why. In the following discussion, I will attempt to summarize the data that we have at hand, and at least explore the questions of how and under what circumstances these clades entered the marine realm, and perhaps by looking at the commonalities among these groups, we can get at least a hint as to why.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

Materials

Mammals have entered the aquatic environment on at least seven separate occasions. The first to do so were the Cetacea and Sirenia, which both originated at approximately the same time in the late Early Eocene (Gingerich, 2005b; Gheerbrant et al., 2005a, b). The earliest cetaceans are known from Indo-Pakistan, while the earliest sirenians are known from Jamaica. Slightly younger sirenians are also found in the Old World. The next group to enter the marine realm was the Pinnipedia, the earliest of which are known from the late Oligocene deposits of the Pacific Northwest (Berta et al., 1989; Koretsky and Sanders, 2002). Desmostylia, a clade of semiaquatic herbivores, are known from North Pacific deposits and lived from the earliest Oligocene to the late Miocene (Domning, 2001b; Barnes and Goedert, 2001). Next were a group of semiaquatic sloths known from the Pliocene of South America (Muizon et al., 2003). Finally, both polar bears and sea otters are known from the modern fauna, but do not have a significant fossil record. These are both thought to be very recent entries into the aquatic environment. These fossils, particularly the earliest of them, and their modern descendants form the basis on which we interpret their lifestyles.

Marine Mammal Diversity

Living groups of marine mammals vary greatly in their diversity. Rice (1998; Table 1 therein) reports that living Cetacea include 83 species in 39 genera; living Pinnipedia include 36 species in 21 genera; and Recent Sirenia include 5 species in 3 genera. Since then, several new species of cetaceans have been described, as well as additional genera, but not all of these new taxa have been widely accepted. The polar bear (Ursus maritimus) and sea otter (Enhydra lutris) are also often included in the marine mammals, which constitute additional diversity and two additional invasions of the aquatic habitat within the order Carnivora in addition to the Pinnipedia (Berta et al., 2006). Species level identification of most fossils is problematic, so most studies of diversity of extinct organisms are done at the genus level. Including both fossil and recent cetaceans, there are around 245 genera described thus far, with around 32 genera of sirenians and around 62 genera of pinnipeds. At particular times in the past, (e.g., the middle Miocene) generic diversity of cetaceans was approximately double what it is today. This finding emphasizes the need to include data on the past diversity and distribution of taxa when attempting to understand their diversity and distribution today. Figure 1 compares the diversity of Cetacea, Sirenia, and Pinnipedia over their fossil histories and in the Holocene, or Recent times.

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Figure 1. Histograms showing the past generic diversity of: A: Cetacea. B: Sirenia. C: Pinnipedia. Note that each of these groups shows times in the past where generic diversity surpassed that of today.

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Methods

Taphonomic studies and years of collecting have demonstrated that most soft tissue of animals decays very rapidly, and for the most part, fossils of vertebrates are usually skeletons and teeth, or more often only fragments of skeletons and teeth. Soft tissue preservation, while rare, does occur. Several instances of baleen preservation have been noted (e.g., Brand et al., 2004), but no other soft tissues of fossil marine mammals have been reported. Thus, any interpretation of the behavior of fossil marine mammals must be reflected in the morphology of the skeleton or teeth, be reflected in modification of the skeleton or teeth, or be interpreted from the depositional context of the fossils. Luckily, many behaviors are directly reflected in these parts of the body with high preservation potential, allowing paleontologists to reconstruct a reasonably clear picture of the lives of extinct marine mammals (Uhen, 2004, for example). Data from studies using morphological and geochemical fossil analysis techniques are presented. The following sections will outline some evolutionary changes affecting the sensory systems, locomotion, breathing, feeding, and reproduction in Cetacea, Sirenia, Desmostylia, and Pinnipedia, and then compare them with each other to see if there are any common patterns among the different groups.

RESULTS

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

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.

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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).

DISCUSSION

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED

Before comparing the evolutionary histories of each of the clades of marine mammals, it is worth emphasizing that the evolutionary histories outlined here are only the most basic and superficial sketches of the morphological changes that these groups have undergone. Within Cetacea alone there are animals that have pachyosteosclerotic ribs and bones not unlike sirenians (Eocetus, Uhen, 1999, 2001), animals that have skulls that resemble those of walruses (Odobenocetops, Muizon, 1993, Muizon et al., 2002), and animals that resemble mammalian crocodiles (Ambulocetus, Thewissen et al., 1994; Remingtonocetus, Kumar and Sahni, 1986). So, while this study focuses on the earliest lineages of these groups, note that they are all much more diverse both in numbers of taxa and in form.

Let us compare the degree to which each of these clades has adopted an aquatic lifestyle. Both Cetacea and Sirenia originated at about the same time and were fully aquatic by the end of the Eocene (see Fig. 3). Desmostylia and Pinnipedia are both semiaquatic. It is difficult to even speculate about how much time or what activities desmostylians performed in the water. The one behavior that we are relatively sure about is feeding. The isotopic study of Clementz et al. (2003) clearly demonstrated that at least Desmostylus fed in the water. Modern pinnipeds perform most of their activities in the water and mainly haul out onto ice or dry land for breeding, bearing, and raising young.

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Figure 3. Phylogenetic trees of marine mammals. A: Cetacea. B: Tethytheria, including Sirenia and Desmostylia. C: Pinnipedimorpha (including Pinnipedia). Important transitions in the evolutionary history of each group are noted. Heavy lines indicate the stratigraphic range of each group, whereas thin lines indicate phylogenetic links and/or ghost lineages.

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Each of these evolutionary histories is different from the others in the order in which changes in each anatomical system occurred. Despite this finding, they all have one change in common at the very beginning. The earliest members of each of these clades of marine mammals show adaptations of the feeding apparatus for feeding in water. For example, the earliest cetaceans have elongate rostra with their incisors along the rostral body, the earliest pinnipeds have a simplified dentition compared with other arctoids (Mitchell and Tedford, 1973), and the earliest sirenians have a narrow forceps-like snout for selective browsing of aquatic or nearshore vegetation (Savage et al., 1994). All of the isotopic studies performed to date are also consistent with this interpretation of the morphology. Also, the two recently evolved marine mammals, the polar bear and sea otter, spend most of their time in the water feeding. This is no great surprise, because a great deal of mammalian evolution has been linked to changes in feeding ecology.

It is also interesting to note that the clades of marine mammals seem to have originated at two discrete times, Cetacea and Sirenia during the early Eocene, and Desmostylia and Pinnipedia during the Oligocene. The Eocene has been noted as a time of high productivity in aquatic environments, with warm, broad, shallow seas (Lipps and Mitchell, 1976; Gingerich et al., 1983) that could have provided abundant resources for early cetaceans and sirenians to exploit.

The Oligocene was very different. Rapid glaciation near the Eocene/Oligocene boundary changed global oceanic circulation dramatically, and tremendously increased the temperature gradient from the equator to the poles (DeConto and Pollard, 2003). Productivity in the Oligocene oceans, like today, was more concentrated than in the Eocene, and was high around areas of upwelling. The origin of the earliest desmostylians and pinnipeds may be tied to exploitation of these concentrated areas of productivity in the Oligocene (Lipps and Mitchell, 1976).

In summary, aquatic characteristics evolved in mosaic patterns, and different morphological solutions to aquatic conditions were achieved separately in each clade. The earliest representatives of each clade all show morphological features that indicate they were feeding while in the water, suggesting that feeding ecology is a key factor in the evolution of marine mammals.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. CETACEAN PHYLOGENY
  4. SIRENIAN AND DESMOSTYLIAN PHYLOGENY
  5. MARINE CARNIVORE PHYLOGENY
  6. WHY DID MARINE MAMMALS GO BACK TO THE SEA?
  7. MATERIALS AND METHODS
  8. RESULTS
  9. DISCUSSION
  10. LITERATURE CITED
  • Arnason U, Gullberg A, Janke A. 2004. Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene 333: 2734.
  • Barnes LG, Goedert JL. 2001. Stratigraphy and paleoecology of Oligocene and Miocene desmostylian occurrences in Western Washington State, USA. Bull Ashoro Mus Paleontol 2: 722.
  • Berta A. 1991. New Enaliarctos (Pinnipedimorpha) from the Oligocene and Miocene of Oregon and the role of “enaliarctids” in pinniped phylogeny. Smithsonian Contrib Paleobiol 69: 133.
  • Berta A, Wyss AR. 1994. Pinniped phylogeny. Proc San Diego Soc Nat Hist 29: 3356.
  • Berta A, Ray CE, Wyss AR. 1989. Skeleton of the oldest known pinniped, Enaliarctos mealsi. Science 244: 6062.
  • Berta A, Sumich JL, Kovaks KM. 2006. Marine mammals - evolutionary biology. 2nd ed. Amsterdam: Elsevier-Academic Press. 547 p.
  • Brand LR, Esperante R, Chadwick AV, Porras OP, Alomía M. 2004. Fossil whale preservation implies high diatom accumulation rate in the Miocene-Pliocene Pisco Formation of Peru. Geology 32: 165168.
  • Cassens I, Vicario S, Waddell VG, Balchowsky H, Van Belle D, Ding W, Fan C, Lal Mohan RS, Simões-Lopes PC, Bastida R, Meyer A, Stanhope MJ, Milinkovitch MC. 2000. Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proc Natl Acad Sci U S A 97: 1134311347.
  • Clementz MT, Hoppe KA, Koch PL. 2003. A paleoecological paradox: the habit and dietary preferences of the extinct tethythere Desmostylus, inferred from stable isotope analysis. Paleobiology 29: 506519.
  • Davis CS, Delisle I, Stirling I, Siniff DB, Strobeck C. 2004. A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. Mol Phylogenet Evol 33: 363377.
  • DeConto RM, Pollard D. 2003. Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2. Nature 421: 245249.
  • Deméré TA, Berta A, McGowen MR. 2005. The taxonomic and evolutionary history of fossil and modern balaenopteroid mysticetes. J Mammal Evol 12: 99143.
  • Domning DP. 2001a. The earliest known fully quadrupedal sirenian. Nature 413: 625627.
  • Domning DP. 2001b. Evolution of the Sirenia and Desmostylia. In: MazinJM, BuffrénilVd, editors. Munich: Verlag Dr. Friedrich Pfeil. p 151168.
  • Domning DP. 2001c. Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. Palaeogeogr Palaeoclimatol Palaeoecol 166: 2750.
  • Domning DP. 2002a. Desmostylia. In: Encyclopedia of marine mammals. San Diego: Academic Press. p 319322.
  • Domning DP. 2002b. The terrestrial posture of desmostylians. Smithsonian Contrib Paleobiol 93: 99111.
  • Domning DP, Buffrénil Vd. 1991. Hydrostasis in the Sirenia: quantitative data and functional interpretations. Mar Mammal Sci 7: 331368.
  • Domning DP, Gingerich PD. 1994. Protosiren smithae, new species (Mammalia, Sirenia), from the late middle Eocene of Wadi Hitan, Egypt. Contrib Mus Paleontol, University of Michigan 29: 6987.
  • Domning DP, Ray CE, McKenna MC. 1986. Two new Oligocene desmostylians and a discussion of tethytherian systematics. Smithsonian Contrib Paleobiol 59: 155.
  • Emlong DR. 1966. A new archaic cetacean from the Oligocene of northwest Oregon. Bull Oregon University Mus Nat Hist 3: 151.
  • Flynn JJ, Finarelli JA, Zehr S, Hsu J, Nedbal MA. 2005. Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Syst Biol 54: 317337.
  • Fordyce RE. 2002. Neoceti. In: PerrinWF, WürsigB, ThewissenJGM, editors. Encyclopedia of marine mammals. San Diego: Academic Press. p 787791.
  • Geisler JH. 2001. New morphological evidence for the phylogeny of Artiodactyla, Cetacea, and Mesonychidae. Am Mus Novitates 3344: 153.
  • Geisler JH, Sanders AE. 2003. Morphological evidence for the phylogeny of Cetacea. J Mammal Evol 10: 23129.
  • Geisler JH, Uhen MD. 2003. Morphological support for a close relationship between hippos and whales. J Vertebrate Paleontol 23: 991996.
  • Geisler JH, Uhen MD. 2005. Phylogenetic relationships of extinct Cetartiodactyls: results of simultaneous analyses of molecular, morphological, and stratigraphic data. J Mammal Evol 12: 145160.
  • Gheerbrant E, Domning DP, Tassy P. 2005a. Paenungulata (Sirenia, Proboscidea, Hyracoidea, and relatives). In: RoseKD, ArchibaldJD, editors. The rise of placental mammals. Baltimore: The Johns Hopkins University Press. p 84105.
  • Gheerbrant E, Sudre J, Tassy P, Amaghzaz M, Bouya B, Iarochène M. 2005b. Nouvelles données sur Phosphatherium escuilliei (Mammalia, Proboscidea) de l'Eocéne inférieur du Maroc, apports à la phylogénie des Proboscidea et des ongulés lophodontes. Geodiversitas 27: 239333.
  • Gingerich PD. 2005a. Aquatic adaptation and swimming mode inferred from skeletal proportions in the Miocene desmostylian Desmostylus. J Mammal Evol 12: 183194.
  • Gingerich PD. 2005b. Cetacea. In: RoseKD, ArchibaldJD, editors. The rise of placental mammals. Baltimore: Johns Hopkins University Press. p 234252.
  • Gingerich PD, Wells NA, Russell DE, Shah SMI. 1983. Origin of whales in epicontinental remnant seas: new evidence from the early Eocene of Pakistan. Science 220: 403406.
  • Gingerich PD, Smith BH, Simons EL. 1990. Hind limbs of Eocene Basilosaurus: evidence of feet in whales. Science 229: 154157.
  • Gingerich PD, Domning DP, Blane CE, Uhen MD. 1994a. Cranial morphology of Protosiren fraasi (Mammalia, Sirenia) from the middle Eocene of Egypt: a new study using computed tomography. Contrib Mus Paleontol, University of Michigan 29: 4167.
  • Gingerich PD, Raza SM, Arif M, Anwar M, Zhou X. 1994b. New whale from the Eocene of Pakistan and the origin of cetacean swimming. Nature 368: 844847.
  • Gingerich PD, Haq MU, Zalmout IS, Khan IH, Malakani MS. 2001. Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293: 22392242.
  • Koretsky IA, Holec P. 2002. A primitive seal (Mammalia: Phocidae) from the Early Middle Miocene of Central Paratethys. Smithsonian Contrib Paleobiol 93: 163178.
  • Koretsky IA, Sanders AE. 2002. Paleontology of the Late Oligocene Ashley and Chandler Bridge Formations of South Carolina, 1: Paleogene Pinniped Remains; The oldest known seal (Carnivora: Phocidae). Smithsonian Contrib Paleobiol 93: 179183.
  • Kumar K, Sahni A. 1986. Remingtonocetus harudiensis, new combination, a Middle Eocene archaeocete (Mammalia, Cetacea) from western Kutch, India. J Vertebrate Paleontol 6: 326349.
  • Lipps JH, Mitchell E. 1976. Trophic model for the adaptive radiations and extinctions of pelagic marine mammals. Paleobiology 2: 147155.
  • MacFadden BJ, Higgins P, Clementz MT, Jones DS. 2004. Diets, habitat preferences, and niche differentiation of Cenozoic sirenians from Florida: evidence from stable isotopes. Paleobiology 30: 297324.
  • Madar SI. 1998. Structural adaptations of early archaeocete long bones. In: ThewissenJGM, editor. The emergence of whales. New York: Plenum Press. p 353378.
  • Mitchell ED. 1989. A new cetacean from the late Eocene La Meseta Formation, Seymour Island, Antarctic Peninsula. Can J Fish Aquat Sci 46: 22192235.
  • Mitchell ED, Tedford RH. 1973. The Enaliarctinae: a new group of extinct aquatic carnivora and a consideration of the origin of the Otariidae. Bull Am Mus Nat Hist 151: 203284.
  • Muizon Cde. 1982. Phocid phylogeny and dispersal. Ann S Afr Mus 89: 175213.
  • Muizon Cde. 1993. Walrus-like feeding adaptation in a new cetacean from the Pliocene of Peru. Nature 365: 745748.
  • Muizon Cde, Domning DP, Ketten DR. 2002. Odobenocetops peruvianus, the Walrus-Convergent Delphinoid (Mammalia: Cetacea) from the Early Pliocene of Peru. Smithsonian Contrib Paleobiol 93: 223261.
  • Muizon Cde, McDonald G, Salas R, Urbina M. 2003. A new early species of the aquatic sloth Thalassocnus (Mammalia, Xenarthra from the late Miocene of Peru. J Vertebrate Paleontol 23: 886894.
  • O'Leary MA, Geisler JH. 1999. The position of Cetacea within Mammalia: phylogenetic analysis of morphological data from extinct and extant taxa. Syst Biol 48: 455490.
  • O'Leary MA, Uhen MD. 1999. The time of origin of whales and the role of behavioral changes in the terrestrial-aquatic transition. Paleobiology 25: 534556.
  • Rice DW. 1998. Marine mammals of the world. Special Pub Soc Mar Mammal 4: 1231.
  • Sanders AE, Barnes LG. 2002. Paleontology of the Late Oligocene Ashley and Chandler Bridge Formations of South Carolina, 3: Eomysticetidae, a new family of primitive mysticetes (Mammalia: Cetacea). Smithsonian Contrib Paleobiol 93: 313356.
  • Savage RJG, Domning DP, Thewissen JGM. 1994. Fossil Sirenian of the west Atlantic and Caribbean region. V. The most primitive known sirenian, Prorastomus sirenoides Owen, 1855. J Vertebrate Paleontol 14: 427449.
  • Simpson GG. 1945. The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85: 1350.
  • Tedford RH, Barnes LG, Ray CE. 1994. The early Miocene littoral ursoid carnivoran Kolponomos: systematics and mode of life. Proc San Diego Soc Nat Hist 29: 1132.
  • Thewissen JGM, Hussain ST, Arif M. 1994. Fossil evidence for the origin of aquatic locomotion in archaeocete whales. Science 263: 210212.
  • Thewissen JGM, Roe LJ, O'Neil JR, Hussain ST, Sahni A, Bajpai S. 1996. Evolution of cetacean osmoregulation. Nature 381: 379380.
  • Thewissen JGM, Williams EM, Roe LJ, Hussain ST. 2001. Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413: 277281.
  • Uhen MD. 1998a. New protocetid (Mammalia, Cetacea) from the late middle Eocene Cook Mountain Formation of Louisiana. J Vertebrate Paleontol 18: 664668.
  • Uhen MD. 1998b. Middle to Late Eocene Basilosaurines and Dorudontines. In: ThewissenJGM, editor. The emergence of whales. New York: Plenum Press. p 2961.
  • Uhen MD. 1999. New species of protocetid archaeocete whale, Eocetus wardii (Mammalia, Cetacea), from the middle Eocene of North Carolina. J Paleontol 73: 512528.
  • Uhen MD. 2001. New material of Eocetus wardii (Mammalia, Cetacea), from the middle Eocene of North Carolina. Southeast Geogr 40: 135148.
  • Uhen MD. 2004. Form, function, anatomy of Dorudon atrox (Mammalia, Cetacea): an Archaeocete from the Middle to Late Eocene of Egypt. University of Michigan Museum of Paleontology Papers on Paleontology 34: 1222.
  • Uhen MD, Gingerich PD. 2001. New genus of dorudontine archaeocete (Cetacea) from the middle-to-late Eocene of South Carolina. Mar Mammal Sci 17: 134.
  • Van Valen LM. 1966. Deltatheridia, a new order of mammals. Bull Am Mus Nat Hist 132: 1126.
  • Wyss AR. 1988. Evidence from flipper structure for a single origin of pinnipeds. Nature 334: 427428.