Adaptive Evolution of Sea Lions and Walruses

Charles A. Repenning

Systematic Zoology, Vol. 25, No. 4. (Dec., 1976), pp. 375-390.

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ADAPTIVE EVOLUTION OF SEA LIONS AND WALRUSES

Abstract Repenning, Charles A., ( U S . Geological Survey, 345 Middlefield Road, Menlo Park,

CA 94025) 1976. Aclaptive evolution of sea lions and walruses. Syst. Zool. 25:375-390.- T h e order Otarioidea includes t w o living and t w o extinct families. O f these four, t h e extinct Enaliarctidae were ancestral t o t h e others and were derived from canoid fissiped carnivores. Th is family, which was most diverse f rom 22 t o 16 million years ago, rapidly developed t h e locomotor, cerebral, and olfactory adaptations t o marine l i fe . T h e extinct Desmatophocidae and t h e extant Odobenidae (walruses ) and Otariidae ( s e a lions ) evolved f rom t h e Enaliarctidae at di f ferent t imes and i n the order i n which t h e y have b e e n mentioned. Each o f these three went through their period o f greatest diversity i n t h e same order; t h e Otariidae o f today represent t h e period o f greatest diversity o f this family. Each o f these three independently developed similar dental, vascular, and social adaptations t o marine existence but i n di f ferent ways. All families were native t o t h e North Pacific. T h e odobenids alone entered t h e North Atlantic through t h e Central American Seaway about 8 million years ago, and t h e otariids alone invaded the southern hemisphere b y 5 million years ago.

There are at least eight types of marine organized for designated rookery breeding adaptations recognizable to some degree and pupping, but still are well adapted in the skeletal morphology of the marine to the two fundamental conditions of pinni- carnivores of the North Pacific Ocean, the ped existence. Thus Bartholomew failed sea lions and the walruses. These adapta- to make note of the poorly understood dif- tions involve hearing, seeing, smelling, eat- ference between what I shall call coastal ing, oxygen conservation, body heat con- and pelagic marine feeding. In the hypoth- servation, locomotion, and behavior in both esis that follows, pelagic feeders, because social and environmental contexts. As of their wide dispersal over the surface noted by Bartholomew (1970) in his ana- of the ocean, survive as a species only lytical hypothesis of the evolution of of through the evolution of a very specific pinniped polygyny, each adaptive special- homing instinct: thus designated rookeries: ization has an effect on others and develops thus male competition for females: thus in harmony with others so that, viewed in dimorphism and pinniped polygyny as its entirety, the complete adaptive system reconstructed by Bartholomew. Coastal is a complex of adaptations with reinforc- marine feeders have a ready access to ing feedbacks between each. As an exam- land or ice; they may haul out in groups ple, differences in diet have markedly influ- at any time of the year but their grouping enced the different skeletal adaptations of is protective rather than for birth and the ears of sea lions and walruses (Repen- breeding; they have evolved relatively in- ning, 1972). significant homing instinct and dimor-

Bartholomew clearly identified two fun- phism; and they do not have designated damental conditions of pinniped existence rookeries for breeding and pupping. The which led to polygyny in seals-terrestrial exception is the walrus, a dimorphic coastal birth and marine feeding-and he outlined feeder whose ancestors, as we shall see, the secondary requirements which built were pelagic feeders. upon these two conditions and, through The hypothesis that breeding behavior feedbacks upon themselves to form an in seals is ultimately directed by feeding adaptive system that led to the evolution patterns is here taken as a logical explana- of pinniped polygyny. He did not address tion of observed differences in two major his analysis to seals that are not socially pinniped life styles and in two major pin-

SYSTEMATIC ZOOLOGY

niped morphologic patterns. Rookery breeding and sexual dimorphism are not related to major phylogenetic patterns in the pinnipeds. Both differences are present in both major pinniped groups, the phocoid seals and the otarioid seals, but with con-fusing exceptions. Variations in the degree of sexual dimorphism are most extreme in the phocoid seals; the living otarioid seals appear to be uniformly dimorphic in sexes, although they were not always so in the past. Intuitively one feels that not enough is yet known of the life history of the seals to explain the observable differences. The

THE FOSSIL RECORD

The known history of the sea lions and the walruses begins about 22 million years ago with a marine carnivore described by Mitchell and Tedford (1973) and named by them Enalkrctos mealsi. These authors placed Enaliarctos in the new subfamily Enaliarctinae of the family Otariidae. How- ever, in their usage this family includes both the sea lions and the walruses, differing from almost all current classifica- tions of the seals in which the sea lions and the walruses are placed in different fam- ilies, the Otariidae and the Odobenidae.

hypothesis clearly is an over~implication.~In the present discussion, therefore,Bartholomew's subtle logic linking rook-

ery breeding to sexual dimorphism was based upon his own extensive observations of living pinnipeds and he recognized (1970, p. 546) that there was little paleon- tologic evidence of the evolution of sexual dimorphism in seals except that one pub- lished fossil record indicated that it is a character of great antiquity. Of the two major groups of seals, the otarioids. are most uniformly dimorphic and, since the time of Bartholomew's work, two reports have been prepared which show, in satis- factory detail, the evolutionary history of the sea lions and walruses based upon the fossil record. One, by Mitchell and Ted- ford (1973), describes the first known member of an extinct otarioid family with many fissiped characters which clearly was the origin of the sea lions and walruses. The second, by Repenning and Tedford (in press), describes the fossil record of the sea lions and walruses from this ances- tral family to those living today. With these as background, and following the logic of Bartholomew, the adaptive evolution of the sea lions and walruses can be discussed as an historic event.

l Although I read Ian Stirling's report (1975) in manuscript prior to the Guelph Symposium in 1972, in the years to pass before its publication I confess that I forgot it. It was published after this report was written and thus was brought back to my attention too late to be considered without major revision. I believe that his dif-ferentiation between aquatic and terrestial mating is sig-nificant and one of the factors which make the presenthypothesis is an oversimplication.

Enaliarctos is placed in the family Enali- arctidae and the enaliarctids are ranked taxonomically equal to the sea lions and the walruses, as was done by Mitchell and Tedford, but considered to be of familial rank as is done in most classifications.

The Enaliarctidae and their derivatives, including a second extinct family named the Desmatophocidae (Hay, 1930) and the living families Otariidae and Odobenidae, comprise the known marine carnivores of the North Pacific, the otarioid seals. The phocoid seals clearly originated in the Atlantic Ocean, to judge from available fossil records. These Atlantic marine carni- vores dispersed to the Pacific at relatively recent dates. Available information sug-gests that the ancestors of the North Pacific sea otter, Enhydra lutris, adopted a marine existence between 6 and 4 million years ago (Repenning, 1976) and can hardly be considered more than terrestrial carnivores with marine habits.

The Enaliarctidae Although the only enaliarctid species

that has been studied and described to date is Enaliarctos mealsi (Mitchell and Ted- ford, 1973), there are a number of speci- mens of several species that have yet to be studied. These are primarily in the National Museum of Natural History in Washington, D. C. (Emlong Collection; C. E. Ray, oral commun., 1973), but some are also in the Los Angeles County Mu-

SEA LIONS AND WALRUSES

seum of Natural History (L. G. Barnes, written commun., 1975) and in The National Science Museum in Tokyo (Y. Hasegawa, oral commun., 1974). The family appears to have been widespread in the North Pacific and to have existed from at least 22 to about 16 million years ago. E. m a l s i is the oldest known member of the family.

As Repenning and Tedford (in press) define the Enaliarctidae, they were otarioid seals having heterodont dentition like that of fissiped carnivores. In E. mealsi the dentition is somewhat similar to that of living canids. The enaliarctids possess up- per and lower carnassial teeth and more or less molariform molars. At that time when any lineage of the enaliarctids evolved the homodont dentition of the de- rived otarioids it crossed the taxonomic boundary into a derived family, by this definition.

Mitchell and Tedford have pointed out the similarity of E. mealsi to early ursids. While derivation from the amphicynodon- tine ursids seems obvious, an enaliarctid with distal limb structures intermediate between flippers and feet has not yet been found, or at least recognized, as all known limb elements possibly belonging to enali- arctids appear to be from well-developed flippers.

The enaliarctids and their descendant families have greatly enlarged orbits in comparison to those of related fissipeds. In the living seals this trait is least developed in the walrus, although it is more obvious in some of its ancestors. I t is generally assumed that enlarged orbits are an aid to vision in underwater conditions of little light, but the explanation of what sort of aid they provide is somewhat obscure (Jamieson and Fisher, 1972). Neverthe-less indirect evidence is convincing; in ad- dition to being an almost universal pin-niped feature, Bryden (1972) has noted that the most rapid growth of the eye of the southern elephant seal occurs when the animal first goes to sea as a pup, weeks after birth.

The lack of pneumatic frontal sinuses is

by no means confined to the pinnipeds as these features are lacking in nearly all aquatic carnivores as well as many small land carnivores. Interestingly, Savage (1957, p. 172) reports that small nasal sinuses are present in the otherwise aquat- ically adapted fossil canoid Potamotherium. Nevertheless, the presence of pneumatic frontal sinuses is a decided handicap to any diving mammal, as most human swim- mers have noted when diving while in-fected with a cold, and Elulliarctos had none.

Reduction of the size of the olfactory fossae, and hence the olfactory lobes of the brain, is a pinniped trait relative to the condition in fissipeds. Mitchell and Ted- ford report a marked reduction in size of the olfactory lobes of Enuliarctos mealsi. The reduction of the olfactory lobes in pinnipeds, including Enuliarctos, seems to parallel reduction of the ethmoturbinates, loss of frontal pneumatic sinues, narrowing and elongation of the interorbital area, posterior placement and squaring off of the anterior part of the brain case, and enlargement of the orbits. Loss of pneu- matic sinuses and enlargement of the orbits are positive specializations of diving mam- mals. The advantages of the other modi- fications, including that of the olfactory lobes, seem obscure, except that they spatially accommodate the development of large orbits and facilitate the loss of pneu- matic sinuses. The reduction of the ethmo- turbinates and of the olfactory lobes ap- pears to have little disadvantage in view of the relative uselessness of smell in the marine environment. The development of these features is obvious in Enaliarctos, although it is not as extreme in many pinnipeds.

Adaptation to the heat-dissipating aquatic environment is a more extreme problem for marine mammals than for freshwater mammals. This is partly be-cause there is less opportunity in the ocean to haul out for grooming and drying, but largely the problem is more critical in marine adaptation because of the greater

depth to which marine mammals must dive. In shallow water the air trapped in the underfur performs efficiently as an insulat- ing blanket but this blanket is rapidly com- pressed by the pressure of greater diving depths, with proportionate decrease in insulating efficiency. Thus dense underfur is a terrestrial and shallow-water adaptation retained, in adults, by only a few marine mammals.

With the possible exception of the sea otter, which perpetuates shallow-water habits in the marine environment and whose existence is dependent upon per-petual grooming, all marine mammals have evolved a blanket of incompressible sub- cutaneous fat and, to varying degrees, large size to better retain body heat.

By fissiped standards the enaliarctids were of medium size; E. mealsi was some- what larger than the larger living otters. But by pinniped standards, particularly in comparison to the walruses and sea lions which derived from them, the enaliarctids were very small. I t seems possible that in- crease in body size, for heat conservation, may have begun in the enaliarctids, but it had not progressed very far.

Storage of a large volume of blood in enlarged venous sinuses and emphasis on circulation to the brain are two major specializations of the sea lions and walruses that permit prolonged apnea while diving. Mitchell and Tedford (1973) have com-mented on the enlarged venous drainage of the brain and the relatively enlarged posterior lacerate foramina of Enaliarctos mealsi, suggesting that this might indicate diving adaptation.

Although adaptations to prolong apnea, enabling prolonged dives, seem to have evolved in Enaliarctos, there appears at first glance to be little modification of the ancestral fissiped ear. E. meab i has a fis- siped-like fossa beside the promontorium for the origin of the tensor tympani muscle, canoid-like inflated auditory bullae, small fissiped-like petrosals, and small ossicles, to judge from the size of the epitympanic recess.

SYSTEMATIC ZOOLOGY

However, Mitchell and Tedford note that the tympanic membrane is very small; approximate measurements suggest an area ratio between the tympanic membrane and the oval window of the cochlea near that of the living sea lions, which is markedly different from that of fissiped carnivores and living walruses. Repenning (1972) has correlated such a ratio with habitual deep diving and has suggested that its effect is to protect the cochlea from exaggerated hydrosonic pressure in deep diving.

In addition, the round window of the cochlea in E. mealsi has an underhanging shelf of petrosal bone, producing a recess for the round window membrane that is referred to as the round window fossa. This fossa is believed to serve as a protec-tive device, shielding the round window membrane from the cavernous tissue which lines the middle ear cavity in living seals and which distends with venous blood in response to increasing hydrostatic pressure, thus equalizing the middle ear pressure with the ambient pressure while diving.

The fissiped-like features of the ear of E. mealsi lack those pinniped modifications that Repenning (1972) interpreted as being advantageous to directional hearing under water. Externally the mastoid, squamosal, and exoccipital regions show no tendency toward developing specifically oriented surfaces for maximum reception of bone-conducted sound waves from specific direc- tions. Internally the lack of enlargement of the petrosal apex suggests minimal adap- tation for greater sensitivity to such bone- conducted sound. In addition, such de-vices as seen in modern seals that are inferred to mute bone-conducted sound from nonspecific parts of the skull, as in- complete fusion of skull elements, appear to have been completely undeveloped in E. m a b i .

Thus, while the circulatory system of the brain and some features of the ear of this earliest otarioid seal suggest that it had evolved deep diving capabilities, Enaliarctos mealsi shows almost no ad-vances toward perfecting directional hear-

SEA LIONS AND WALRUSES

ing under water. The adaptive features improving directional hearing under water follow different patterns of specialization in those families derived from the enaliarc- tids (Repenning, 1972) and might, there- fore, be expected to have developed little in the enaliarctids.

The pinniped families derived from the Enaliarctidae, although not their earliest representatives, all show strong sexual di- morphism, suggesting the breeding behav- ior of the modern sea lions. Bartholomew ( 1970) has tied sexual dimorphism, at least that dimorphism in which the males are markedly larger and stronger than the females, to rookery pupping and to some form of "harem" breeding. These animals must leave their pelagic life for a period each year and return to an established rookery for breeding. Presumably estab- lished rookeries lead to concentration of individuals, concentration leads to com-petition for females by the males, and male competition leads to dimorphism.

Little or no evidence is known so far that indicates sexual dimorphism in the enaliarctids and all specimens of E. mealsi are of the same approximate size. Lack of apparent dimorphism suggests habits more similar to those living coastal-feeding seals that inhabit the waters marginal to land or ice, who haul out frequently, and who have not evolved sexual dimorphism be- cause of male competition resulting from crowding at designated rookeries.

The persistence of fissiped-like dentition in the enaliarctids argues even more strongly for close ties with the shore. Shearing and chewing teeth have little use for eating in water for, while the first bite that has been cut from the prey is being masticated, the rest floats away. The heterodont dentition of the enaliarctids certainly suggests that they may have fre- quently hauled their catch ashore to eat. In animals tied this closely to the shore, rookery instinct, with its consequent crowd- ing, male competition, and sexual dimor- phism, is not needed to sustain breeding and pupping.

Homodont dentition seems to have de- veloped in seals as a consequence of the abundance of small prey in the marine environment that could be swallowed whole. In contrast to the needs of terres-trial carnivores, there is no need in the sea to rely upon prey that is too large to be swallowed and so must be cut into pieces. Nevertheless, unquestionable shear wear on the carnassial teeth of the earliest enaliarctids indicates that they did cut their prey into pieces, suggesting that they did prey on animals too large to swallow. Why they did not rely entirely on the abundant small prey is difficult to understand, but it may indicate a relatively inefficient stage of swimming adaptation, a possibility not yet verified by study of their skeletal structure, or possibly a hunting deficiency related to their lack of directional hearing under water.

Thus the enaliarctids, ancestors of the sea lions and the walruses, may be pictured as small flippered animals, probably with a dense underfur such as is retained in liv- ing fur seals. They were coastal marine feeders with enlarged orbits for underwater vision and with circulatory and ear special- izations that permitted prolonged and deep dives. However, it seems reasonable to suppose that, unlike modern seals, they fre- quently hauled their prey ashore to eat it and, because of this affinity to the shore, had not developed rookery behavior. Directional sensitivity to underwater sound was not developed, and they probably re- lied entirely upon their enlarged eyes to locate their food and their surroundings. They were derived more than 22 million years ago from terrestrial ursids and re-tained in dentition and in skull structure many features of these early ursids, as shown by Mitchell and Tedford (1973), but they were highly successful and appear to have inhabited the entire coastal area of the North Pacific Ocean until about 16 million years ago.

The Desmatophocids This small, extinct, but formerly abun-

dant and widespread group of otarioid

SYSTEMATIC ZOOLOGY

seals was the first of the three families to arise from the enaliarctids by the evolution of homodont dentition. This transition took place 16 to 17 million years ago, and the desmatophocids survived until about 9 mil- lion years ago. They are known from Cali- fornia, Oregon, Japan, and questionably from Alaska (Repenning and Tedford, in press). Only two genera are recognized, Desmatophoca (Condon, 1906) and Al-lodesfnus (Kellogg, 1922); however, the latter genus contains three recognized spe- cies and the former may contain two, although only one is currently recognized. Barnes (1972) has recently reviewed the family.

In comparison to the enaliarctids, the desmatophocids show a great increase in size, considerable modification of the ear region, and sexual dimorphism, as well as homodont dentition. If the interpretations made here are valid, the desmatophocids had become adapted to pelagic life and were not tied to the behavior pattern of the coastal feeders.

In size, the desmatophocids were com-parable to the living sea lions. In modi- fication of the ear structure, the des-matophocids had reduced inflation of the auditory bullae and thickened bullar walls, adaptations that are believed to reflect greater directional sensivity to sound in water. The jugular process of the exoccipi- tal was greatly expanded into a postero-lateral projection, but the mastoid process was not greatly changed from the enaliarc- tid condition. Although only moderately enlarged, the petrosal was modified in form and its internal acoustic meatus was very wide in comparison to that of fissipeds, enaliarctids, and otariids; there was almost complete separation of the canals for the facial and vestibulocochlear nerves. The tympanic membrane was reduced in size and the auditory ossicles were enlarged. The entire ear structure shows much more specialization than that of the enaliarctids, and many of the modifications have re-sulted in structures that enable directional hearing under water as outlined by Repen-

ning ( 1972). Nevertheless these structures are clearly less developed than they are in sea lions and the walruses; particularly poorly developed were major flat areas on the skull favoring sound reception from selected directions.

As noted in the publications of both Mitchell (1966) and Barnes (1972), the desmatophocids, particularly Allodesmus but including Desmatophoca, had remark- ably large orbits in comparison with the sea lions and particularly the walruses of to- day. This condition, in combination with the rather minimal adaptation to direc-tional hearing under water, suggests that these descendants of the enaliarctids may have perpetuated the enaliarctid use of more sensitive vision to overcome the lim- ited perception in the underwater environ- ment.

Although having homodont crowns, the cheek teeth of Desmatophoca were multi-ple rooted. In most species of the more advanced genus Alloclesmus the teeth were single rooted, presumably resulting from increased simplicity of the crowns. This trend toward single roots on the cheek teeth was subsequently repeated in the evolution of both the walruses and, later, the sea lions. Although it is difficult to imagine a reason for the apparent coinci- dence, the development of single-rooted cheek teeth in the desmatophocids, odo-benids, and otariids seems to mark, in the fossil record, the beginning of great diversification and abundance of the family.

At the time of their greatest diversity, from about 14 to 12 million years ago, the desmatophocids, then represented pri-marily by species of the genus Allodesmus, lived in association with the earliest of the odobenids and the last of the enaliarctids. These odobenids were no more than half the size of the then-abundant des-matophocids and the enaliarctids were even smaller. There can be no question of the adaptive superiority of the desmatophocids at this time. However, by the time of their latest fossil records, which are few in num-

SEA LIONS AND WALRUSES

ber, the desmatophocids are found with abundant and very large odobenids and the earliest otariid seals. These early otariids were very small and differed from their enaliarctid ancestors in little more than their homodont dentition; heterodont enaliarctids had vanished from the North Pacific by this time through evolution into the more advanced otaroid families. Shortly after the disappearance of the des- matophocids the odobenids began their period of great diversity.

The desmatophocids were thus the first family of the advanced otarioid seals to evolve from the enaliarctids. In addition to having homodont dentition, they were large and were sexually dimorphic suggest- ing that they had abandoned hauling their food ashore to eat, that they had com-pletely overcome the problems of thermal regulation and were not dependent on hauling out for grooming and drying, and that they had adopted a pelagic life and rookery breeding. Their greatly enlarged orbits and minimal adaptation to direc-tional hearing underwater suggest that they may have concentrated on their eyes for underwater orientation as did their ancestors, the enaliarctids. Nevertheless they were very successful seals and in-habited the North Pacific Ocean for some 8 million years.

T h e Walruses

The family Odobenidae has been the most abundant and diversified group of the North Pacific marine carnivores and except for a period of about three million years, has lived continuously in this oceanic basin for the last 14 million years. Living and extinct genera of odobenids constitute about half of the named genera of non-phocid seals known from the North Pacific. In addition, the odobenids were the only group of otarioid seals that dispersed to the North Atlantic, where two additional ex-tinct genera are recognized.

The oldest form here considered to be an odobenid is about 14 million years old and has been assigned to the genus Neo-

therium (Kellogg, 1931). I t is one of the most poorly known named otarioid seals and its dentition is unknown. Mitchell and Tedford (1973) consider Neotherium as a possible enaliarctid. However, the known postcranial bones of Neotherium, although primitive, are distinctly odobenid, and many elements resemble miniature replicas of those of highly specialized walruses 2 million years younger. In addition, L. G. Barnes (oral commun., 1975) has collected enough topotypic postcranial material to indicate that Neotherium was sexually di- morphic, and adaptation so far not known in the enaliarctids.

Although here presumed to have had homodont dentition, and hence to be an odobenid rather than an enaliarctid, Neo-therium was little or no larger than Enaliarctos mealsi.

The next younger fossil odobenid was Imagotaria downsi Mitchell ( 1968), a species that was remarkably abundant along the west coast of North America from 12 to possibly 9 million years ago. This species is one of the most completely known named extinct otarioid seals (Re-penning and Tedford, in press). I t was the size of a modern walrus, was sexually dimorphic to an extreme degree, had homodont dentition similar to modern sea lions, and had specializations of the ear that, while being clearly odobenid, indicate that it had sea lion-like feeding habits. It was a deep-diving pelagic feeder with a well-developed rookery-type breeding be-havior. One fossil locality in Santa Cruz, Californa, where the remains of Imugotaria downsi are very abundant, appears in many respects to represent nearshore deposits adjacent to an ancient rookery according to Repenning and Tedford (in press).

As mentioned, the postcranial bones of Imagotaria downsi resemble those of Neo-therium except that they are much larger. The teeth of I. downsi are so variable in the presence or absence of multiple roots that it seems clear the known sample shows the transition to single-rooted cheek teeth. All later walruses have single-rooted cheek

382

teeth. All later walruses appear to be de- rived from I. downsi, for this species is known from far more localities than is any other extinct pinniped species and there are no other odobenids known at the time of Imagotaria downsi. There is one record of the last of the desmatophocids ("Des- matophocine A of Barnes, 1972) and numerous records of the first and smallest of the otariids that have been found with Zmagotaria downsi, but this modern-sized odobenid was the dominant seal of the North Pacific for longer than any other known species of seal. Immediately after this long span of Imagotaria downsi, and its development of single-rooted cheek teeth, odobenid diversification bloomed as the desmatophocids had diversified 6 mil-lion years earlier and as the otariids would diversify 6 million years later.

Between 8 and 4 million years ago no less than seven odobenine genera are known from the North Pacific. They represent a variety of adaptive types; some remained active pelagic predators as Zmagotaria and others appear to have pro- gressively adapted to a shallow-water mol- luscan diet as seen in modern walrus. In the latter we see an interesting mixture of retained primitive features along with the evolution of other characters reflecting shallow-water adaptations. Thus the liv-ing walrus retains the sexual dimorphism developed at least 12 million years ago in Zmagotaria downsi but has experienced a major degeneration of the rookery breed- ing behavior that produced it. Ray and Watkins (1975) briefly describe the breed- ing behavior of Odobenus bulls as one of courtship by swimming adjacent to the hauled-out females rather than haulings out themselves and establishing a breed-ing territory. These authors suggest that the bulls, in addition to advertising their availability, may establish a form of under- water territory, but rookery behavior as seen in modern otariids and as inferred in the ancestral odobenid Imagotaria cer-tainly is not present.

Similarly, shallow-water habits appear

SYSTEMATIC ZOOLOGY

to have led to an enlargement of the tym- panic membrane in modern walrus and in extinct forms that adopted a bottom-feed- ing diet. Their tympanic membranes are larger than those of Zmugotaria or, in fact, Enaliarctos and the ratio betwen the area of the membrane and that of the oval win- dow is closer to that of some land mammals than it is to that of the deep-diving ances- tors of the walrus (Repenning, 1972, Table 1).

A comparable change in the reduction of the size of the orbits is seen in the pro- gression leading to Odobenus; the advan- tage of both of these "reversed evolution" trends may be the improvement of these senses in air when deep-water adaptations are no longer needed. Hypothetically, therefore, living walruses should have bet- ter hearing and vision in air than living sea lions, though there has been no testing of this hypothesis.

This complex of odobenid seals is divisi- ble into two subfamilies which are defined, fundamentally, by the relative enlargement of the upper and lower canine teeth (Re- penning and Tedford, in press). Charac-ters distinguishing the two subfamilies are found throughout their skeletons, however. The canines of both were enlarged ulti- mately into tusks. The subfamily Dusig- nathinae shows this enlargement in both upper and lower canines, the genus Dusignathus (Kellogg, 1927) being the most extreme example so far described. The subfamily Odobeninae, in contrast, had reduced lower canines while the uppers evolved into tusks, the living genus Odo- benus being an obviously extreme example of this specialization.

All known odobenine odobenids appear to have been or to be bottom feeders but the dusignathine odobenids, which have been extinct for the last three to four million years, include both pelagic and bottom feeders.

Except for the living walrus, only the oldest of the odobenine odobenids, as yet unnamed (see Repenning and Tedford, in press), is known from the North Pacific

SEA LIONS AND WALRUSES

and its distribution was southerly. I t is known from Baja California, and one record in this area is south of the Tropic of Cancer. More than 5 million and pos- sibly as much as 8 million years ago this odobenine, or an unknown but closely re- lated form, passed into the Atlantic Ocean by way of the Central American Seaway between Central and South America. In the Atlantic, and in the absence of sibling competition but in association with the well-diversified phocoid seal fauna of that ocean, odobenine odobenids evolved into the modern bottom-feeding walrus as indicated by an ample fossil record extend- ing back about 5 million years. The oldest record of modern walrus in the North Pa- cific is from Alaska and is probably less than one million years old; it seems most likely, therefore, that the subfamily re-turned to the Pacific by way of the Arctic Ocean.

In the North Pacific the dusignathine odobenids are known from Baja California to Oregon; none are yet known from the western Pacific area. Although the sub-family contains species that appear to have been pelagic feeders, some of the named genera have been found in situations that strongly suggest they were bottom-feeding shallow-water animals, and, in fact, two genera are known only from ancient inland seas and have no record from the former open coastal area of the eastern North Pacific.

Following the time of Imagotaria downsi the otariid seals became larger and more abundant; it may be that their rise to prominence during the diversification of the Pacific odobenids had a directing ef- fect on the adaptational developments of these odobenids and that by this time of odobenid diversification the otariids had already gained supremacy in the pelagic environment, a supremacy once enjoyed by Imagotariu downsi.

Aside from the living genus Odobenus, introduced less than one million years ago from the Atlantic, the youngest records of odobenids from the North Pacific basin are

from the ancient inland sea of central Cali- fornia. Two genera are involved: Plio-pedia (Kellogg, 1921) and Valenictus ( Mitchell, 1961 ), both of which are poorly known but both of which were most likely molluscivorous bottom feeders and are known only from deposits in the ancient inland seas. The youngest record is that of the genus Valenictus and is from the Ket- tleman Hills in California; this record is somewhat older than 4.3 million years (Repenning and Tedford, in press ) .

The extinction of the dusignathine odo- benids in the North Pacific would seem to have left the molluscivorous marine carnivore niche unoccupied, for the otariid seals did not take it over as they did pelagic feeding. However, Repenning (1976) has noted that the oldest marine occurrence of the ancestors of the North Pacific sea otter is from beds that contain Pliopedia in the Kettleman Hills and that these ancestors, showing progressive development toward the living molluscivorous sea otter, are present, in the same area, in beds contain- ing the latest record of Valenictus and in younger strata. It may be that the end of 10 million years of odobenid history in the North Pacific resulted in another fissiped carnivore entering the sea, enaliarctid-like, and occupying the shallow-water mollus- civorous niche left vacant by the last of the dusignathine odobenids.

The odobenids were thus the second family of the advanced otarioid seals to evolve from the enaliarctids. Although fol- lowing the same pattern of marine adapta- tion, their history differs in some respects from that of the desmotophocids. Large size, for heat conservation, and sexual di- morphism, presumably indicating pelagic feeding and rookery breeding, appear at the same time in the record of the des- matophocids. This may merely reflect the incompleteness of the fossil record. In the odobenids it appears that dimorphism pre- cedes the development of large size. There- fore, large size, while advantageous, is not mandatory for pelagic feeding. As will be discussed, this is even more obvious in the

otariids. Nevertheless large size developed early in odobenid history, as shown by the genus Imagotaria, and has remained a fea- ture of all known odobenids since that time. The degree of dimorphism and the size have remained constant in nearly all genera since Imagotaria, although some undescribed specimens indicate that there have been a few exceptions. There would appear to be some optimal control of these two features.

With respect to directional hearing underwater, the odobenids seem intermedi- ate in specialization between the earlier desmatophocids and the later otariids, but they developed their specialization at an early stage; the fundamental odobenid ear structure was fully established in Imago- taria and the only differences between the ear of this early odobenid and that of the living walrus are exaggerations of these structures and, as mentioned, the "reverse evolution" of some, which appears to have resulted from the adoption of shallow-water bottom feeding.

Although the desmatophocids had a greatly exaggerated jugular process of the exoccipital bone for reception of water-borne sound to be conducted through the skull to the ear, the odobenids have a very small jugular process, even less prominent than in Enaliarctos mealsi. On the other hand, the odobenids have an exaggerated mastoid process of the temporal bone that forms a prominent posterolateral-facing sur- face for the same purpose as the en-larged jugular process in the desmatopho- cids and the desmatophocids, as noted, show no specialization of ;the mastoid process. Enlargement of the mastoid process continued progressively from the Imagotaria condition and is much more conspicuous in later odobenids.

The auditory ossicles of Imagotaria are essentially identical to those of Odobenus and presumably all odobenids. The petrosal is also essentially identical in all known odobenids except that enlargement of its apex appears to have been a progres- sive development. I t is interesting to note,

SYSTEMATIC ZOOLOGY

however, that this progressi0.n appears to have been more rapid in pelagic forms as the petrosal apex of Imagotaria is actually more enlarged than that of some later bottom-feeding walruses.

The history of the odobenids may be summarized as one of rapid evolution into the highly successful pelagic feeder Imago- taria downsi followed by diversification of forms, dispersal into the North Atlantic, and orientation toward bottom feeding in association with the phocoid fauna of the North Atlantic and with the evolving otariid fauna of the North Pacific. In the Pacific the family became extinct and within the Atlantic evolution was markedly unidirectional toward the living walrus, which returned to the Pacific basin as a highly specialized bottom feeder less than one million years ago.

The Sea Lions The family Otariidae includes those

seals usually referred to as the sea lions and the fur seals. These two forms have been considered as belonging to two separate subfanlilies on the basis of the presence of abundant underfur in the fur seals and little of it on the sea lions. Repenning, Peterson, and Hubbs (1971) cast doubt on the subfamilial distinction because of their inability to find definitive characters other than the underfur and subsequent work on the endemic louse fauna of the otariids (Kim, Repenning, and Morejohn, 1975) and on the otariid fossil record (Re- penning and Tedford, in press) has estab- lished rather conclusively that the two genera included in the subfamily of the fur seals, Callorhinus and Arctocephalus, are less closely related to each other than Arc- tocephalus is related to the living genera of sea lions. Therefore the subfamilial break- down of the Otariidae should no longer be recognized.

As with the walruses, the sea lions and the fur seals acquired homodont dentition well before evolving large size. In fact the smallest of the living fur seals, the Galapa- gos fur seal, is not greatly larger than was

-- 385 SEA LIONS AND WALRUSES

Enaliarctos mealsi and most living fur seals are only nloderately larger. In comparison to the great variety of forms found in the other otarioid families, especially the odo- benids, the otariids have gone through very little diversification until very recent time. In correlation with this, some living otariids still retain some double-rooted cheek teeth.

The earliest known otariid, Pitlzanotaria starri, is about 11 million years old and was very small, it was smaller than Enali-arctos mealsi but had homodont dentition. Although known from a number of locali- ties, its remains at each locality are, in most cases, represented by only a few bones and there is no known complete and well-pre- served skull. This form is recognizable as an otariid largely because of the character of its postcranial skeletal elements although some of these, particularly those of the manus, are so primitive that they might not be so recognized if they had not been found in association with other skeletal ele- ments. Nevertheless, only size and minor differences in form separate most of the postcranial bones of this earliest otariid from those of living otariids. In describing the holotype of Pitlzanotaria starri, a con- temporary of Znzagotaria dozunsi, Kellogg (1925) compared it quite favorably with the living Alaskan fur seal. As a generality, it can be said that little more than the loss of heterodont dentition separates the early otariids from the enaliarctids and little more than the loss of multiple-rooted cheek teeth separates them from the living otariids. It is not surprising, therefore, that Mitchell and Tedford ( 1973), in comparing Enaliarctos mealsi with other pinnipeds, found the greatest number of similarities in the sea lions and particularly the fur seals.

If Pithanotaria was sexually dimorphic, the degree of dimorphism was slight as all specimens known appear to be from in- dividuals of about the same size. All later otariids have very distinctive supraorbital processes in adult males but no specimen of Pithanotaria demonstrates the presence of such processes, again suggesting that the

genus was characterized by little sexual dimorphism. It is here suggested that this earliest otariid may have been a coastal feeder and that the family had not yet evolved pelagic-rookery behavior. Pos-sibly the spectacular success of the malrus- sized Zmagotaria downsi as a pelagic feeder during the time of Pitllanotaria had some influence on the behavioral evolution of this minute otariid.

About 8 million years ago there were otariids in the North Pacific that definitely showed an increase in body size, had flip- per bones that, while still primitive in some respects, were unmistakably otariid, showed massive supraorbital processes on the skulls of the males, and were clearly sexually dimorphic to a degree equal to living otariids. Except for slight differences in some of the limb elements and for the retention of double-rooted cheek teeth, these forms could easily be taken for mod- ern sea lions. Despite the modern aspect of these sea lions, diversification was almost nonexistent. Most fossil otariids from about 8 to perhaps 4 million years ago have been placed in one genus and only tw7o species are recognized (Repenning and Tedford, in press). Additional undescribed species existed in Japan (Y. Hasegawa, oral com- mun., 1974). The specific differences recognized represent some modernization of limb elements and possibly enlargement of the venous storage of blood, enabling more prolonged periods of diving.

A single mandibular fragment is known of an individual that lived midway between 8 and 4 n~illion years ago and that shows the beginning of single rootedness in otariid cheek teeth. The specimen also shows features suggesting closest affinity to the Alaskan fur seal. Additional speci- mens of about 5, 4, and 3 million years ago appear to be allied to this form and show increasing resemblance to the Alaskan fur seal in dentition, basicranial features, and brain structure. During this time dou- ble-rooted cheek teeth persist in what is be- lieved to be the main otariid lineage lead- ing to the southern fur seal and to the sea

lions. It is therefore believed that the liv- ing Alaskan fur seal belongs to a lineage that diverged from the main otariid stem about 6 million years ago.

Also during this time, about 5 million years ago according to available state-ments of their age, the otariids dispersed southward to the southern hemisphere and are reported from deposits of this age in Peru (R. Hoffstetter, written commun., 1973). As they did not at this time enter the Atlantic, it is presumed that the Cen- tral American Seaway was closed at least to the passage of otariid seals.

The earliest known large otariid with all cheek teeth single rooted, comparable in specialization to the living sea lions, is from beds in Japan of about 2 million years age (Kaseno, 1951). This sea lion is assigned to the living genus Eumetopias, although it is believed to be a species dif- ferent than that living today (Mitchell, 1968). In the eastern Pacific a single femur, now in the University of California Museum of Paleontology, from deposits at Capitola, California (D. Domning, oral commun., 1975), may represent a similarly ancient large sea lion. The femur is very large, is between 4 and 3 million years old, and was found in association with the ancestors of the Alaskan fur seal.

Specimens representing extinct species of living sea lion genera are known from slightly younger rocks in both Japan and North America, and fossil representatives of living sea lion and fur seal species have been found in rocks deposited within the last million years in both North and South Pacific areas. It is presumed, therefore, that the living sea lion genera evolved from the Arctocephalus-like otariid stem between two and three million years ago by a rather abrupt acceleration of trends toward in-creasing size and single-rooted cheek teeth.

Thus the otariid seals evolved out of their enaliarctid ancestors 12 to 13 million years ago with little change other than the development of homodont dentition. At first they appeared to perpetuate the enali- arctid-like coastal feeding habits and were

SYSTEMATIC ZOOLOGY

neither large nor sexually dimorphic. How- ever about 8 million years ago, at about the same time that the odobenids began to diversify and to show considerable adapta- tion towards shallow-water bottom, rather than pelagic, feeding, the otariids became larger, sexually dimorphic, and rookery-breeding seals. These otariids had per-fected all of the specialized adaptations of modern otariids and differed from them only in their degree of development of these adaptations. Their evolution until about 3 to 2 million years ago was un-diversified and slight except for a diver-gence, about 6 million years ago, of a lineage that led to the living Alaskan fur seal. In the past two million years there has been considerable acceleration in increase in size, development of single-rooted cheek teeth, and diversification of genera. The southern fur seal genus Arc- toceplzalus represents the otariid prototype and spread to the southern hemisphere at least 5 million years ago; there it has di- versified into six southern species which are distributed entirely around the world in the southern seas. The sea lions, the most recent development of the otariids, appear to have spread to the southern hemisphere less than three million years ago and these have dispersed only into the western South Atlantic from the South Pacific.

SUMMARY OF ADAPTIVE EVOLUTION

Of the eight marine adaptations recog- nizable to some degree in the skeletal morphology of the sea lions and walruses, six are evident in the ancestral enaliarctids. Of these six adaptations, two clearly were incomplete in terms of the adaptation as developed in the living seals. These two further evolved in the three descendant families along with these two adaptations not known in the known enaliarctids. The evolution of these marine adaptations is here summarized in the approximate order of their appearance in the fossil record.

Locomotion.-Though the fossil record is very incomplete, limb bones from the

SEA LIONS AND WALRUSES

same deposits as skulls of the earliest enali- arctids suggest that they had well-developed flippers with short and strong proximal elements and elongate distal ele- ments. Subsequent modification of flipper structures occurred and the flippers of the three derived familes are distinguishable because of these modifications. In addition, early and later stages of evolution within each family may be recognized by relative modernization of the bones of the flippers. But it appears that one of the first of the marine adaptations was the development of pinniped locomotion, and this seems to have been developed at least 22 million years ago.

Underwater uision.-The enlarged orbits of the pinnipeds are evident in the earliest enaliarctid, Enaliarctos mealsi. This adap- tation is possibly as unique among canoid carnivores as is that of flippers; although many canoids, particularly mustelids, are aquatic, none have developed large orbits. This in itself suggests tha't large orbits are not simply an aquatic adaptation but re-flect, instead, deep diving. Secondary re- duction of the orbits in modern walrus, following the adoption of a shallow-water bottom-feeding habit, further suggests that large eyes are a deep-diving adaptation.

The desmatophocids, first of the three families to evolve from the enaliactids, have even larger orbits, presumably en-abling better use of limited light. The walruses and the sea lions, on the other hand, show little change in the enaliarctid orbital size but rather show improved directional sensitivity to underwater sound for orientation to their surroundings.

Oxygen conseruation.-This adaptation, of obvious advantage to prolonged diving, is one of the soft anatomy, including blood composition, and leaves little skeletal evi- dence. The principal skeletal evidence lies in enlarged blood circulation to the brain, which is imprinted on the internal wall of the braincase and hence is evident in fossil endocranial casts. I t is also indicated in the relative size of the vertebral foraminia which house enlarged venous sinuses.

From internal brain casts (Mitchell and Tedford, 1973) it appears that Enaliarctos mealsi was alreadv well ada~ted to the apnea required fo; prolonged-dives. This interpretation appears to be consonant with that of enlarged orbits being related to deep diving and with specializations of the ear of Enaliarctos mealsi.

Nevertheless, Repenning and Tedford (in press) note apparent enlargement of the vertebral foramina in the lineage of the sea lions as recentlv as the ~ e r i o d from 8 to 5 million years agd. From ihis it seems reasonable to suppose that though oxygen conservation was well developed in Enuli- arctos mealsi some 22 million years ago, the adaptation was continually improved upon in the sea lions and walruses.

Olfaction.-As has been mentioned, re-duction of the size of the olfactory lobes of the brain is a pinniped character to be found in Enaliarctos meahi. Correlated with this character are the reduction of the ethmoturbinates and their withdrawal posteriorly in the interorbital area, narrow- ing and elongation of the interorbital area, loss of pneumatic sinuses if these were not already lost in the freshwater fissiped ances- tors of the enaliarctids, posterior placement of the anterior portion of the braincase and squaring off of its anterior corners, and enlargement of the orbits.

It is not evident at Dresent if reduction in olfaction is a marin; adaptation of the seals or if it is a loss of a relatively useless sense as a consequence of enlargement of the orbits and the resulting posterior posi- tioning of the mandibular musculature. Whatever the selective pressure may have been, reduction in size of the olfactory lobes has been documented in Enuliarctos mealsi by Mitchell and Tedford (1973), and this reduction appears as great in this ancestral species as in most modern sea-

lions and walruses. Hearing.-The osseous structure, and

the soft anatomy that can be inferred from it, of the ear region in the otarioid seals may easily be broken down into two func- tions: protection against pressure and

388

sensitivity to sound.' Several features of the ear of Enalircrctos mealsi indicate that adaptations were present that protected this delicate structure from extreme hydro- static pressure, again suggesting that this early otarioid was a deep diver. However, virtually no structures are present that indi- cate a directional sensitivity to water-borne sound. A few features of the des-matophocid ear suggest some directional sensitivity perhaps 16 million years ago but it was only in the sea lions, at least 8 mil-lion years ago, and the walruses, at least 12 million years ago, that this sensitivity was fully developed.

It is herein suggested, largely upon the basis of the ratio of the areas of the tym- panic membrane and the oval window, that those odobenids that adopted a shallow-water bottom-feeding life style lost some of the protective adaptations for deep div- ing evident in earlier odobenids and in the earliest enaliarctid.

Heat conservation.-As with oxygen con- servation, heat conservation is primarily an adaptation of the soft anatomy. The only skeletal evidence that appears to reflect this adaptation is large body size and for the most part this appears to have been an accomplishment of the families derived from the enaliarctids. Some of the living otariids appear to have made little progress in this particular direction from the enali- arctid condition. However, the odobenids achieved large size 12 million years ago and the desmatophocids did so 16 million years ago.

Feeding behavior.-It appears that the enaliarctids, as this ancestral family is de- fined, were coastal feeders and it has been suggested that the earliest forms frequently may have eaten prey too large to swallow and hauled their prey ashore to dismem- ber and eat it, as was done by their fissiped ancestors. From the fossil record it seems that once homodont dentition was de-veloped and derived families came into existence, all otarioids rapidly adopted pelagic feeding, for larger size, suggesting better heat conservation, and sexual dimor-

SYSTEMATIC ZOOLOGY

phism, suggesting well-established rookery breeding, quickly follow homodonty in the development of the desmatophocids, odo- benids, and otariids. Generic diversifica- tion followed next in all derived families.

The odobenids are unique among the de- scendants of the enaliarctids in that they evolved forms adapted to shallow-water bottom feeding after adapting to pelagic feeding. Orientation toward this feeding habit may have been influenced by the spectacular pelagic success of Imugotaria downsi and its pelagic descendants and by the deveropment of pelagic otariids during the diversification of the odobenids. In the North Atlantic, this orientation toward bot- tom feeding in the immigrant walruses may have been encouraged by the well- diversified endemic phocoid fauna.

Social behavior.-Bartholomew ( 1970) has pointed out that, unlike fissiped carni- vores, the "feeding behavior and breeding behavior [of pinnipeds] are not only spatially separated, they occur in com-pletely different habitats." Although this has removed consideration of food supply from breeding behavior, it is the thesis of this paper that feeding habits have had and have a marked effect on breeding be- havior. All seals return to land or ice to bear their pups, and they breed at this time either on the land or in adjacent water. This is not a problem to seals that feed primarily along the coast or ice front and that are not great wanderers. But the need to get the population together for the breeding season has caused a major selec- tion bias toward those with homing in- stincts in seal populations that disperse widely over the pelagic environment to feed and that engage in major seasonal dispersal patterns. Thus the emphasis on the desire to return to the place of birth has produced the rookery breeding be-havior in pelagic feeders and rookery behavior has resulted in crowding at selected breeding areas, in males contesting for females, and in selection for more powerful males and sexual dimorphism. All of the otarioid seals evolved sexual di-

SEA LIONS AND WALRUSES

morphism except the ancestral Enaliarc-tidae. The enaliarctids were small coastal feeders showing no sexual dimorphism and hence are not believed to have been rook- ery breeders. They lived at least from 22 to about 16 million years ago.

The desmatophocids are first known about 16 million years ago as large, sexually dimorphic forms believed to have been rookery breeders and pelagic feeders. The fossil record is not complete enough to state that they acquired these characters at the same time as homodont dentition.

The first odobenid, of about 14 million years ago, was small but appears to have been sexually dimorphic and hence is thought to have been a pelagic feeder and a rookery breeder. Within the next two million years the odobenids evolved large size and clearly were rookery breeders. By 8 million years ago some odobenids had at least begun to adapt to shallow-water bottom feeding. Though the breeding be- havior characteristics of rookery breeding presumably began to deteriorate, culminat- ing in the extent of deterioration seen in living walrus, sexual dimorphism, which rookery breeding produced according to the reasoning of Bartholomew, has been re-tained in the bottom-feeding walruses.

The first otariids of about 12 million years ago were small and not sexually di- morphic; they are presumed to have re-tained the coastal feeding habits of the enaliarctids. The otariids became distinctly sexually dimorphic by 8 million years ago, and some were clearly larger than the enaliarctids. However, it was not until about 3 million years ago that some otariids attained the large size of the living sea lions and a few living otariids still retain small size; one is almost as diminutive as were the enaliarctids.

Though there is some variation in the order of development, there is a general trend in the adaptive evolution of the three seal families derived from the enaliarctids. The trend is away from the coastal feeding habits of the enaliarctids to pelagic feeding and related breeding patterns. Homodonty,

improved oxygen conservation, underwater hearing, sexual dimorphism, and large size all developed or improved in each of the derived groups, in some cases in different ways, and in each family at distinctly dif- ferent times as each family evolved out of the enaliarctids and replaced the earlier one. Thus the great dominance and diver- sity of the living otariids represents the same sort of diversity as that of the odobe- nids between 8 and 5 million years ago, and that of the desmatophocids 16 to 14 million years ago.

ACKNOWLEDGMENTS

This discussion is an outgrowth of the work Richard H. Tedford and I have done in document-ing the fossil history of the otarioid seals and I thank him for years of constructive discussion. George A. Bartholomew, Francis H. Fay, Bumey J. LeBoeuf, and Edward H. Miller have reviewed the manuscript at various stages and have made many helpful suggestions, most profitable to me because of my lesser familiarity with seal behavior.

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