The name Pinnipedia was first proposed for fin-footed car’ nivores more than a century ago. Pinnipeds—fur seals and sea lions, walruses, and seals—are one of three major clades of modern marine mammals, having a fossil record going back at least to the late Oligocene [27 to 25 millions of years before present (Ma)]. The earliest pinnipeds were aquatic carnivores with well-developed paddle-shaped limbs and feet. A North Pacific origin for pinnipeds has been hypothesized; the group subsequently diversified throughout the worlds oceans.
I. Pinniped Ancestry: Origin and Affinities
There has long been debate about the relationship of pinnipeds to one another and to other mammals. The traditional view, also referred to as diphyly, proposes that pinnipeds originated from two carnivore lineages, an odobenid (walrus) plus otariids (fur seals and sea lions) grouping affiliated with ursids (bears) and phocids (seals) being related to mustelids (weasels. skunks, otters, and kin) (Fig. 1A). The current view supported by cladistic analysis of both morphologic and molecular data supports pinnipeds as monophyletic (having a single origin). Although the hypothesis presented here positions ursids as the closest relatives of pinnipeds, it is acknowledged that there is difficult)’ separating the various lineages of arctoid carnivores (mustelids, procyonids, and ursids) at their point of divergence (Fig. IB). Other hypotheses support pinnipeds as either allied with mustelids or as having an unresolved arctoid ancestry.
There is, however, still disagreement about relationships among pinnipeds. Most of the controversy lies in the debate as to whether odobenids are most closely related to phocids or to otariids. Most morphologic data support a link between phocids and the odobenids, whereas molecular data favor a link between odobenids and otariids.
II. Divergence of Major Lineages
The broad pattern of evolution within pinnipeds shows divergence of five major lineages. These include the three extant lineages—Otariidae, Phocidae, and Odobenidae—and two extinct groups—the Desmatophocidae and a basal lineage Ena-liarctos (Berta and Sumich, 1999; Fig. 2). At times the Odobenidae have been included in the Otariidae, although cladistic analysis currently supports these as distinct monophyletic groups.
Within Pinnipedimorpha (living pinnipeds plus their fossil allies) are included archaic pinnipeds Enaliarctos and Pteronarctos + pinnipeds (Fig. 2). Berta and Wyss (1994) established a cladistic diagnosis of the group based on 18 synapomorphies of the skull, teeth, and postcrania. Unequivocal derived features include large infraorbital foramen, anterior palatine foramina anterior of maxillary-palatine suture, upper molars reduced in size, lower first molar metaconid reduced or absent, humerus short and robust, deltopectoral crest on the humerus strongly developed, and digit I on the manus and digit I and V on the pes emphasized. The basal taxon Enaliarctos from the late Oligocene and early Miocene (27-18 Ma; Fig. 3) of California is known by five species, one represented by a nearly complete skeleton (Fig. 4). Enaliarctos was a small, fully aquatic pinni-pedimorph with shearing teeth (as is typical of most terrestrial carnivorans), flexible spine, and fore- and hindlimbs modified as flippers. Several features of the hindlimb suggest that Enaliarctos was capable of maneuvering on land, although it probably spent more time near the shore than extant pinnipeds. Ecologically, the earliest pinnipedimorphs were coastal dwellers that likely fed on fish and other aquatic prey. A later diverging lineage allied more closely with pinnipeds than with Enaliarctos is Pteronarctos from the late Miocene (19-15 Ma) of coastal Oregon. Pteronarctos is recognized as the earliest pinniped to have evolved the unique maxilla diagnostic of modern pinnipeds. The maxilla of pinnipeds makes a significant contribution to the orbital wall. This differs from the condition in terrestrial carnivores in which the maxilla is limited in its posterior extent by contact of several facial bones (jugal, palatine, and/or lacrimal).
Fur seals and sea lions (eared seals), the Otariidae, are diagnosed by frontals that extend anteriorly between the nasals, large and shelf-like supraorbital process of the frontal, secondary spine dividing the supraspinous fossa of the scapula, uniformly spaced pelage units, and the presence of a trachea with an anterior bifurcation of the bronchi (Berta and Sumich, 1999; Fig. 5). Although otariids are often divided into two subfamilies, Otariinae (sea lions) and Arctocephalinae (fur seals), only the sea lions are believed to have descended from an exclusive common ancestor, at least according to morphologic data. The otariids are the earliest diverged pinniped lineage, originating approximately 11-12 Ma (Fig. 3) and including the poorly known Pithanotaria from the late Miocene of California and three species of Thalassoleon described from the late Miocene of California, Mexico, and Japan. Thalassoleon is distinguished from Pithanotaria in its larger size and lack of a thickened ridge of tooth enamel at the base of the third upper incisor (Fig. 6). An extinct species of the Northern fur seal genus, Callorhinus, has been described from the late Pliocene of southern California, Mexico, and Japan. One fossil fur seal from the Pleistocene of Peru of the southern fur seal genus Arctocephalus has been referred to a new subgenus, Arctocephalus (Hydrarctos). Cladistic analysis of otariids by Berta and Demere (1986) recommended that Hydrarctos be elevated to generic status. Several extant species of Arctocephalus have a fossil record extending to the Pleistocene in South Africa and North America (California). The fossil record of modern sea lions is poorly known. The following taxa are reported from the Pleistocene: Neophoca (New Zealand), Eume-topias and Zalophus (Japan), and Otaria (Brazil).
Figure 1 Alternative hypotheses for relationships among pinnipeds. (A) Monophyly with ursids as the closest pinniped relatives. (B) Diphyly in which phocids and mustelids are united as sister taxa as are otariids, odobenids, and ursids.
Figure 2 A cladogram depicting the relationship of the major clades of pinnipeds.
Figure 3 Chronologic ranges of major lineages and genera of extinct and living pinnipeds (time scale in millions of years). Thick lines shotv stratigraphic ranges of taxa and thin lines indicate their phylo-genetic relationships. Branching points are not necessarily correlated with the time scale. Note phocid interrelationships are shown as unresolved due to conflicting molecular and morphologic data sets.
Figure 4 The pinnipedimorph Enaliarctos mealsi showing pinnipedimorph synapomorphies described in the text.
Otariids appear to have originated in the North Pacific (Fig. 7). Sea lions diverged as a distinct lineage between 3 and 5 Ma. Both fur seals and sea lions dispersed to the Southern Hemisphere within the past 3 Ma. The diversification of otariids in the Southern Hemisphere has been attributed to several factors, including increased levels of primary productivity in colder waters, which at this time reached to the equator, and island hopping assisted by favorable currents. Sea lion diversification proceeded subsequent to the isolation of populations in the Northern and Southern Hemispheres of the Pacific basin, leading to divergence of the California, Japanese, and Galapagos sea lions (Zalophus) and Stellers sea lion (Eumetopias) in the north and the Australian sea lion (Neophoca) and southern sea lion (Otaria) and the New Zealand sea lion (Phocarctos) in the south.
Figure 5 Skulls/ventral view of ear regions of (a, d) otariid, (b) walrus, and (c, e) phocid illustrating otariid synapomorphies: frontals extend anteriorly between nasals (contact between these bones is transverse in walruses or V-shaped in phocids) and phocid synapomorphies: pachyostotic mastoid bone (not seen in other pinnipeds) and greatly inflated ectotympanic bone.
Walruses or Odobenidae are diagnosed as a monophyletic group by the presence of a broad, thick pterygoid strut, fourth upper premolar with a strong posterolingually placed proto-cone shelf, lower first molar with the talonid heel absent, and a calcaneum with a prominent medial tuberosity (Fig. 6). Another purported odobenid synapomorphy (i.e., construction of the antorbital process by the maxilla and frontal bones) is now known to be primitive (Demere and Berta, 2001). Morphologic study of the evolutionary relationships among walruses has identified the following taxa: Prototaria, Proneotherium, Neotherium, Imagotaria, dusignathines. and odobenines; the latter includes the modern walrus.
Fossil walruses first appear in the early Miocene (16-18 Ma; Fig. 3) fossil record with Prototaria in Japan and Proneotherium in North America (Oregon). These archaic walruses are characterized by unenlarged canines and narrow, multiple rooted premolars with a trend toward molarization (Fig. 8), adaptations suggesting retention of the fish diet hypothesized for archaic pinnipeds rather than evolution of the specialized mollusc diet for the modern walrus. Portions of the axial and hindlimb skeleton of Proneotherium preserve evidence of a number of aquatic adaptations, including a laterally flexible spine, a broad, shortened femur, and a paddle-shaped foot (Demere and Berta, 2001). In addition to Proneotherium and Prototaria, two monophyletic clades of walruses are recognized that diversified in the late Miocene (Fig. 3). Dusignathine walruses, which include Dusignathus, Pontolis, and Gomphotaria, developed enlarged upper and lower canines. Gomphotaria pugnax, the most completely known dusignathine, is distinct cranially and dentally in its possession of large, procumbent upper lateral incisors and canines; the latter with deeply fluted roots and a small orbit. Odobenines, which include Aivukus, Alachtherium, Valenictus, and Odobenus, evolved the enlarged upper tusks seen in the modern walrus. Unique among pinnipeds is the toothlessness of Valenictus chulavistensis from the late Pliocene of California, presumably an adaptation for suction feeding (Demere, 1994).
Figure 6 Skull of an early otariid, Thalassoleon mexicanus, from the late Miocene of western North America in lateral (top) and ventral (bottom) views. Original 25 cm long.
It has been proposed that the modern walrus lineage (odobe-nine walruses) entered the Caribbean from the Pacific via the Central American Seaway (between 5 and 8 Ma) and dispersed northward into the North Atlantic (Fig. 7). Less than 1 Ma the living genus Odobenus returned to the North Pacific through the Arctic Ocean. Alternatively, on the basis of a new, earlier record of the modem walrus lineage form Japan, it has been suggested that this lineage may have evolved in the North Pacific and dispersed instead to the North Atlantic through the Arctic during the Pleistocene.
The earless seals, the Phocidae, are diagnosed as a monophyletic group by pachyostotic mastoid region, greatly inflated entotympanic bone, complete absence of the supraorbital process of the frontal, strongly everted ilia, and lack of an ability to draw the hindlimbs forward under the body due to a massively developed astragalar process and greatly reduced calcaneal tuber (Wyss, 1988; Fig. 5). Phocids have traditionally been divided into two or four major subgroupings, there is considerable disagreement regarding which are monophyletic. Most molecular and morphologic evidence supports “monachines” (or Monachinae) as early diverging phocids. The Phocinae are universally accepted as monophyletic, although relationships among taxa within this group differ among workers.
Although an earlier, less well-documented record of phocids from the late Oligocene of South Carolina exists (Koret-sky and Sanders, in press), there is undisputed evidence for both the “monachine” and phocine seal lineages from the middle Miocene (approximately 15 Ma) on both sides of the North Atlantic. The phocine lineage is represented by Leptophoca, and the “monachine” lineage is represented by Monotherium (Fig. 3). Despite the fact that a number of fossil “monachines” have been described, not all are known by comparable elements. In addition to Monotherium among the better known taxa from eastern Europe are Pontophoca from the middle Miocene and Callophoca from the early Pliocene; both taxa are under study by Koretsky. Several archaic lobodontine (Pphocine) seals (i.e., Arcophoca and Piscophoca) represented by complete skeletons are known from the late Miocene and/or early Pliocene of South America (Peru) and Homiphoca from South Africa (Fig. 3). Acrophoca is unique among phocids with its long, slender skull, flexible neck, and elongated body (Fig. 9). Although these fossil taxa have been referred to the lobodontines, a subgrouping of “monachines,” new discoveries, as well as restudy of material previously referred to these taxa, suggest that they may in fact be more closely related to phocines. The fossil record of extant “monachines” is poorly known and includes only Monachus and Mirounga from the late Pleistocene and the lobodontine Ommatophoca from the late Pliocene (Fig. 3). With regard to fossil phocines among the best known taxa are Prophoca (middle Miocene) in the eastern North Atlantic, Crrjptophoca (late Miocene) in the Black Sea region, and Phocanella (early Pliocene) in both the eastern and the western North Atlantic (Fig. 3). Extant phocine genera with a fossil record include Phoca from the late Pliocene and Erignathus and Histriophoca from the late Pleistocene (Fig. 3).
The purported first appearance of phocids in the North Atlantic suggests that the common ancestor of phocids had migrated to the North Atlantic, either northward through the Arctic Basin or southward through the Central American Seaway (Fig. 7). Support for a southern route is based on the hypothesized close relationship of phocids and the extinct des-matophocids, the latter occurring as far south as Mexico, and the fact that the Bering land bridge blocked access to the Arctic through much of the late Oligocene and early Miocene. The biogeographic history of monk seals (Monachus spp.) is conflicting, as there are differing hypotheses for their phylogenetic position relative to other phocids. Alternative routes show dispersal in both directions through the Central American seaway followed by diversification in the colder waters of the Southern Hemisphere to produce the lobodontine seal fauna of the Antarctic today.
The biogeographic pattern for phocine seals is no less complicated given the different phylogenetic hypotheses proposed. Although it was suggested earlier that phocines were a Northern Hemisphere radiation, a considerable diversity of phocine seals is known from the Southern Hemisphere during the late Miocene and/or earlv Pliocene (assuming that Acrophoca, Homiphoca, and Piscophoca are phocines rather than lobodontine “monachines”)- In addition, other phocine lineages appear to have been isolated in the Paratethys Sea (northern arm of the Tethys Sea stretching across the area now occupied by the Black, Caspian, and Aral Seas of Eurasia) and the North Atlantic during the late Miocene and Pliocene. Several dispersal routes for phocines seem likely. One hypothesized dispersal involved an initial migration from the Paratethys Sea into the
Figure 7 Reconstruction of continents, ocean basins, and paleocoastlines in the (a) early Miocene (20 Ma) (1, early records of archaic pinnipeds, odobenids, and desmatophocids) and (b) middle Miocene (12 Ma) (1, early well-documented. phocids; 2, dispersal of “monachines” and odobenids to Atlantic; 3, dispersal of phocines to South Pacific; and 4, isolation of phocines in remnants of Paratethys Sea and in North Atlantic).
Arctic Basin, followed by an eastward migration to give rise to modern Phoca/Pusa. In this scenario the land-locked Baikal seal (Pusa sibirica) gained access to Lake Baikal from the Arctic via large lakes at the southern margin of the Siberian ice sheet. A second land-locked species, the Caspian seal (Pusa caspica) remained in the Caspian Sea as an isolated remnant of Paratethys as judged by the presence of fossils similar to living Caspian seals in this location. A second dispersal involved a westward migration of the remaining phocines from the North
Atlantic to their current ranges. The hooded seal (Cystophora cristata) occurs at high latitudes of the Atlantic basin and apparently never dispersed successfully to the Pacific. The bearded seal (Erignathus barbatus) is presently confined to the Arctic and sub-Arctic around the North Atlantic, but Pleistocene records extend as far south as Portugal. Another hypothesis argues for a North Atlantic origin for all phocines with glacial events causing speciation. For example, cyclical fluctuations in glacial maxima (with concomitant variations in sea level) through the Pleistocene mediated range expansions of Phoca spp., ultimately leading to the isolation of populations in refugial centers (i.e., Arctic, Okhotsk, Aleutian) and the divergence of populations (e.g., ribbon seal, Histriophoca fasci-ata, ringed seal, Pusa hispida, larga seal, Phoca larga, harbor seal, Phoca vitulina, harp seal, Pagophilus groenlandicus).
Figure 8 Lateral and ventral views of skulls of fossil odobenids. (Left) Imagotaria down si i from the Miocene of western North America. Original 30 cm long. From Repenning and Tedford (1977). (Right) Prototaria planicephala from the Miocene of Japan. Original 27 cm.
An extinct family of archaic pinnipeds, the desmatophocids, are characterized by elongate skulls, relatively large eyes, mortised contact between two cheekbones, and bulbous cheek teeth (Fig. 10). Cladistic analysis has identified the Desmatophocidae, which includes two genera, Desnvitophoca and Allodesmus, as the common ancestors of phocid pinnipeds. This clade, phocids + Allodesmus and Desmotophoca, termed the Phocoidea, is supported by four synapomorphies, including premaxilla-nasal contact reduced, squamosal-jugal contact mortised and marginal process below ascending ramus well developed (Demere and Berta, in press; Fig. 2). This interpretation differs from previous work that recognized desmatophocids as otarioid pinnipeds (a paraphyletic group that includes walruses but excludes phocids). Desmatophocids are known from the early and middle Miocene (23-10 Ma) of the western United States and Japan (Fig. 3). Newly reported occurrences of Desmatophoca confirm the presence of sexual dimorphism and large body size in these pinnipeds (Demere and Berta, in press). Allodesmus is a diverse taxon (as many as six species have been named) with taxa informally divided into “broad headed” and “long headed” subgroups. The previous suggestion that Allodesmus retained a mobile proboscis, much like the modern elephant seal, seems unlikely on anatomical grounds. Allodemus, known by several complete skeletons, retains several features consistent with forelimb propulsion but also displays adaptations for hindlimb swimming (Adam and Berta. 1998).
Figure 9 Skeleton of an archaic phocid, Acrophoca longisrostris, the Miocene of Peru.
Figure 10 Skeleton of the desmatophocid, A Hodesmus keme-nesis, from the Miocene of western North America. Original 2.2 m long.