Tuesday, August 26, 2014

The evolutionary history of walruses, part 2: the larger imagotariines: Pseudotaria, Pelagiarctos, Imagotaria, and Pontolis

For other entries in this series, see:

Walrus Evolution, part 1
Walrus Evolution, part 3
Walrus Evolution, part 4
Walrus Evolution, part 5

The previous post dealt primarily with the earliest diverging walruses – generally speaking, these were the smaller-bodied “imagotariines”. The “Imagotariinae” is a paraphyletic grade consisting of stem-walruses, and existed during the middle and late Miocene. The earliest diverging imagotariines detailed in the previous post include Prototaria, Proneotherium, Neotherium, and Kamtschatarctos. More derived imagotariines include Pelagiarctos from the middle Miocene of California, Pseudotaria muramotoi from the late Miocene of Japan, and Imagotaria downsi from the late Miocene of California and Oregon. Another problematic walrus is the giant Pontolis magnus from the late Miocene of Oregon, which may be an imagotariine, or possibly a dusignathine walrus – but will be discussed here rather than the next post on dusignathines.

Although small-bodied enaliarctine-like imagotariine walruses like Prototaria and Proneotherium are the earliest diverging walruses, the larger-bodied and later diverging walrus Pelagiarctos actually constitutes the earliest record of the family. Specifically, the mandibles of Pelagiarctos that Morgan and I published on in PLOS One (Boessenecker and Churchill, 2013) are from the “Topanga” Formation of Orange County, which is 17.5 Ma at the oldest, and thus either the same age as Prototaria from Japan and Proneotherium from Oregon, or slightly older. This suggests that when they first appear in the early Middle Miocene, there were already three genera of walruses and already a bit of size disparity.

The holotype skull of the imagotariine Pseudotaria muramotoi from the late Miocene of Hokkaido, Japan. From Kohno (2006).

Despite its smaller size and earlier diverging position on the cladogram, Pseudotaria muramotoi appears about 5-7 million years after Pelagiarctos, and was reported from the late Miocene of Hokkaido by Dr. Naoki Kohno (2006). Pseudotaria is intermediate in morphology and geochronologic age between the middle Miocene Neotherium and the late Miocene Imagotaria downsi. The holotype skull of Pseudotaria lacks the front of the rostrum and has no teeth, but is otherwise characterized by a wide and slightly arched palate, double-rooted cheek teeth, a braincase with a rounded lateral margin (e.g. lacking a box-shaped braincase of earlier odobenids and enaliarctines). Pseudotaria is more derived than Neotherium in the loss of a third root on the upper first molar, the loss of a furrow on the lateral side of the braincase corresponding to the pseudosylvian sulcus of the brain, and a slightly arched palate. However, more derived odobenids differ in having a wider and pentagonal basioccipital, and by lacking an upper second molar. Another imagotariine from the same formation representing a new genus is currently being described by my labmate Yoshi Tanaka and Dr. Naoki Kohno.

Specimens of Pelagiarctos sp. from the "Topanga Formation" (A) and Pelagiarctos from the Sharktooth Hill Bonebed (everything else).

Pelagiarctos is known only from a handful of specimens – the holotype of Pelagiarctos thomasi is a fragmentary “chin” consisting of left and right mandibles with poorly preserved teeth from the middle Miocene Sharktooth Hill Bonebed, collected by LACM head preparator Howell Thomas. Barnes (1988) also referred a handful of isolated cheek teeth to Pelagiarctos. Pelagiarctos thomasi is large – at least the same size as Imagotaria if not somewhat larger – and with noticeably larger cheek teeth than Imagotaria. Pelagiarctos thomasi is unique amongst stem walruses in having a fused mandibular symphysis; otherwise, the cheek teeth are double rooted and similar to Neotherium in shape by retaining a metaconid cusp (essentially, the teeth have four cusps), but are also inflated and bulbous, more similar to Imagotaria. Other features shared uniquely with Imagotaria amongst all walruses are the presence of a lingual cingulum (a ridge on the base of the crown along the lingual side – tongue-side – of the tooth) that bears numerous little cusps on it, and a canine that has a longitudinal groove on one side giving it a near figure-8 shaped cross section. Morgan Churchill and I (Boessenecker and Churchill 2013) referred a more completely preserved pair of mandibles with an incisor, canines, and three cheek teeth to Pelagiarctos – but owing to the unfused symphysis, we referred it to Pelagiarctos sp. This specimen also showed that Pelagiarctos primitively retains a second lower molar, like Proneotherium and Neotherium, and some specimens of Imagotaria, and unlike later diverging dusignathine and odobenine walruses. Because of the aforementioned similarities with Imagotaria, our cladistic analysis found that Pelagiarctos and Imagotaria form a clade – and depending upon future analyses, may permit redefinition of a more exclusive and monophyletic Imagotariinae (defined on at least a couple of dental features).

The "split" skull of Imagotaria downsi from the diatomite quarries of Santa Barbara County, referred by Mitchell (1968).

The sea lion-like walrus Imagotaria downsi was originally reported by Ed Mitchell in 1966 from late Miocene diatomite quarries in the vicinity of Lompoc in Santa Barbara County. The holotype specimen is from the latest Miocene Sisquoc Formation, while other nearby quarries yielding fossils of Imagotaria are from the underlying Monterey Formation. The stratigraphy of this area is problematic, as few quarries preserve the formational boundary between the Monterey and Sisquoc Formations, and both units are identical in lithology – meaning that age determinations need to be done using microfossils. Microfossil dates are only available for a couple of quarries – and microfossil dates for some of the more obscure quarries is no longer available, since some of these quarries are now closed and no longer exist.

An immature male skull of Imagotaria downsi from the Santa Margarita Sandstone near Santa Cruz, reported by Repenning and Tedford (1977).

The type specimen of Imagotaria is a partial rostrum and palate with much of an upper dentition, a nearly complete mandible, several isolated teeth, a fragmentary basicranium, atlas, humerus, and some other bits. Mitchell (1966) also referred a well-preserved complete skull (also from Lompoc) split horizontally and exposed in two slabs. I heard recently that during his Ph.D., Ed Mitchell wanted to reassemble the two slabs and prepare the specimen out and use that as the holotype – but then-director of the USNM, Remington Kellogg, would not allow the specimen to be reassembled. So, Mitchell chose the less complete specimen as the holotype. Additional specimens collected later from the Santa Margarita Sandstone in the Santa Cruz Mountains near Santa Cruz and the city of Scotts Valley from a series of sand and gravel quarries include two beautifully preserved skulls, mandibles, postcrania, and a couple of partial articulated forelimbs – all described by Repenning and Tedford (1977) and Barnes (1971). Imagotaria downsi is a relatively large pinniped, approximately the same size as an Australian sea lion (or, intermediate between a California sea lion and the Steller’s sea lion for fellow American readers). Like Pseudotaria, Imagotaria lacks the boxy braincase of earlier imagotariines, but differs from earlier imagotariines (Pseudotaria included) in having anterior premolars that are single rooted. Imagotaria differs from all earlier walruses in possessing a large and cuspate lingual cingulum (like Pelagiarctos) on the upper premolars in addition to having a well-developed protocone cusp on the cingulum. Imagotaria further differs from all earlier walruses in lacking the metaconid cusp on the lower cheek teeth. The available sample of Imagotaria indicates that there is a bit of variability in dental morphology – some specimens have a lower second molar and others do not, while some have two (or three) upper incisors, and there is some variation in postcanine tooth rooting; the available sample also shows evidence of sexual dimorphism. One specimen – a beautiful female skull from the Santa Margarita Sandstone reported by Repenning and Tedford (1977), known affectionately to some as “Rep’s girl”, has proportionally much smaller teeth than other specimens of Imagotaria downsi. A recent conversation with Dr. Naoki Kohno indicated that this specimen may represent a second species of small-toothed Imagotaria.

An adult female skull of Imagotaria from the same locality as the immature male, reported by Repenning and Tedford (1977) and affectionately known as "Rep's girl". This specimen may represent a second small-toothed species of Imagotaria.

Two partial articulated forelimbs (male, left, female, right) of Imagotaria downsi from the Santa Margarita Sandstone near Santa Cruz, including a tiny radius of Neotherium mirum for comparison (in middle); from Repenning and Tedford (1977).

Numerous additional but mostly undescribed specimens of Imagotaria have been reported from other late Miocene localities. Several skulls from the Empire Formation in Oregon represent a younger species of Imagotaria with single-rooted teeth – these specimens were briefly mentioned by Deméré (1994). I’ve seen them in person, and they are beautiful skulls, but much smaller than Imagotaria downsi. In the past few years, I’ve collected a few isolated teeth from the base of the Purisima Formation that are a dead ringer for Imagotaria – they have a cuspate lingual cingulum and a small pseudo-talonid basin, differing from the turnip-shaped teeth of dusignathine walruses (which also tend to lack enamel and have an inflated root). These teeth come from a bonebed that is just shy of 7 Ma, and represent the youngest fossil record of imagotariines anywhere.

The Lomita walrus. This thing is almost the same size as Pontolis and in life was likely just as scary. This fossil needs to be redescribed. From Lyon (1941).

One problematic Imagotaria-like walrus was reported and figured by Lyon (1941) from the late middle Miocene Valmonte Diatomite member of the Monterey Formation near Lomita in Los Angeles County, California. The Lomita walrus is huge - the skull is 56 centimeters long, and constitutes one of the largest described fossil pinnipeds in existence. Unfortunately, the skull is a bit squashed, but appears to have been relatively similar to Imagotaria and undescribed skulls of Pontolis magnus, but noticeably differs from both in exhibiting primarily single rooted teeth, and apparently lacking a cuspate lingual cingulum on the cheek teeth. Although this specimen was referred by Mitchell (1968) to Imagotaria downsi, this fossil is freaking enormous and about 20 centimeters longer than the largest known skulls of Imagotaria, in addition to lacking a cuspate lingual cingulum and a more derived pattern of root fusion. Instead, this monstrous walrus may be conspecific or congeneric with an undescribed and beautifully preserved skull and skeleton from the Capistrano Formation of Orange County known as “Waldo”, currently under study by student Isaac Magallanes at the Cooper Center (and recently highlighted in a recent talk by Isaac, Dr. Jim Parham, and myself at the Secondary Adaptations meeting in D.C.). Because study is still ongoing, I won’t spoil anything, other than just say “Wow” – you won’t be disappointed when it comes out, so stay tuned.

The holotype braincase of Pontolis magnus from the late Miocene Empire Formation of Oregon, photographed at the USNM in Washington D.C. That pinniped was pretty damn huge.

The last imagotariine, and by far the most impressive – is the gigantic walrus Pontolis magnus. Pontolis was described in 1905 by Frederick True, based upon a large braincase from the late Miocene (7-9 Ma) Empire Formation in Oregon. Since then, several specimens including complete and partial skulls, mandibles, and postcrania were referred to Pontolis by Deméré (1994) and one mandible was figured in our Pelagiarctos paper (Boessenecker and Churchill, 2013). Owing to ongoing work by Morgan Churchill and I, I won’t spoil many details other than what’s already been published. Pontolis is a giant imagotariine characterized by a huge nuchal crest on the braincase, large and ventrally flattened tympanic bullae, a long rostrum, incipiently single-rooted anterior cheek teeth, and an elongate mandible with a large digastric insertion and low, elongate coronoid process. Most impressive is the ridiculous size of Pontolis: its skull is 60 cm long, one-third larger than the largest modern walrus, and approaching the length of elephant seal skulls. Deméré (1994) originally found support for Pontolis as a dusignathine walrus, but a cladistic analysis by Kohno (2006) found Pontolis to form a clade with Imagotaria instead. Our cladistic analysis from the Pelagiarctos study found a compromise of sorts between the previous two studies: our results supported Pontolis as appearing one node closer to the “crown” Odobenidae – the Dusignathine + Odobeninae clade, and neither a dusignathine nor a sister taxon of Imagotaria. As always, more imagotariine (and dusignathine) fossils and a longer set of characters are needed to precisely pin down the phylogenetic position of Pontolis. I won’t say anything more, except that after two current otariid projects, Pontolis will likely be the next joint project by Morgan and I.

So, what does all this tell us? In general, late Miocene imagotariines had simpler dentitions, more robust skulls, larger canines (but not tusks, obviously), and more strongly concave (and more elongate) palates than the walruses of the middle Miocene. The late Miocene is notably the period in which the largest walruses existed, with two different forms approaching the size of elephant seals. Curiously, the largest imagotariines like Pontolis appear just as the similarly large desmatophocid Allodesmus became extinct – the youngest known record of Allodesmus is an undescribed skeleton from the late Miocene (9 Ma) Montesano Formation of Washington, USA. I have suspected since I was an undergraduate that imagotariines filled in available niche space after desmatophocids started on their way out.

Imagotariines of the late Miocene - look at that size disparity!  
Neotherium mirum for comparison (top left).

Rock units like the Empire Formation show us that at least two walruses – Imagotaria and Pontolis – were sympatric, and the only other described pinniped known from coeval rocks is the early fur seal Pithanotaria starri, an adorably tiny otariid about the size of a modern Guadalupe fur seal (Arctocephalus townsendi/phillippii). Altogether, this sort of diversity is reminiscent of pinniped diversity during the middle Miocene (e.g. the walruses Pelagiarctos and Neotherium, and the desmatophocid Allodesmus), but doesn’t compare well with the diversity of modern pinnipeds in the eastern North Pacific during the Holocene and late Pleistocene (four otariids and two phocids, as well as the walrus Odobenus straying far south in glacial periods). Notably absent during much of the late Miocene are tusked walruses – the first of which would appear about 7 Ma just before the close of the Miocene. The earliest Dusignathines also appear just before the end of the Miocene (unless Pontolis turns out to be a dusignathine after all). For whatever reason, imagotariines – which appear to reflect dietary generalists like modern sea lions – died out at the end of the Miocene, paving the way for strange tusked beasts with a taste for clams (and squid?). The last imagotariines, represented by a handful of teeth from the base of the Purisima Formation, mark the end of a ten million year dynasty of  generalist sea lion-like walruses – and mark the beginning of something a whole lot weirder.

Next up: the Dusignathines.


L. G. Barnes. 1971. Imagotaria (Mammalia: Otariidae) from the Late Miocene Santa Margarita Formation Near Santa Cruz California. PaleoBios 11:1-10.
R. W. Boessenecker and M. Churchill. 2013. A Reevaluation of the Morphology, Paleoecology, and Phylogenetic Relationships of the Enigmatic Walrus Pelagiarctos. PLoS One 8(1):e5411.

T. A. Deméré. 1994. The Family Odobenidae: A phylogenetic analysis of fossil and living taxa. Proceedings of the San Diego Society of Natural History 29:99-123.

N. Kohno. 2006. A new Miocene odobenid (Mammalia: Carnivora) from Hokkaido, Japan, and its implications for odobenid phylogeny. Journal of Vertebrate Paleontology 26(2):411-421.

G. M. Lyon. 1941. A Miocene sea lion from Lomita, California. University of California Publications in Zoology 47:23-41.

E. D. Mitchell. 1968. The Mio-Pliocene pinniped Imagotaria. Journal of the Fisheries Research Board of Canada 25(9):1843-1900.

C. A. Repenning and R. H. Tedford. 1977. Otarioid seals of the Neogene. Geological Survey Professional Paper 992:1-93.

F. W. True. 1905. Diagnosis of a new genus and species of fossil sea-lion from the Miocene of Oregon. Smithsonian Miscellaneous Collections 48(1):47-49.

Wednesday, August 20, 2014

The evolutionary history of walruses, part 1: Introduction, and the earliest walruses

Note: A bit of a disclaimer is necessary. This will probably be one of my most indulgent post series, as this is probably my most favorite topic in paleontology. Walruses are a totally weird and fascinating group to study, and I hope some of my enthusiasm for these fantastic blubbery beasts shines through. For later entries in this series, see:

Walrus Evolution, part 2
Walrus Evolution, part 3
Walrus Evolution, part 4
Walrus Evolution, part 5

The walrus (Odobenus rosmarus) is one of the most peculiar and charismatic of all modern mammals, and easily the most distinctive of all pinnipeds. The modern walrus is characterized by its great bulk and most obviously by its large tusks; currently the walrus is restricted to the Arctic region, inhabiting the coasts of Greenland, Baffin Island, and Northern Quebec in the Northwestern Atlantic region, Svalbard, Novaya Zemlya, the Barents Sea, and the Laptev Sea in the Arctic region, and the Chukchi Sea and Bering Sea around Alaska and the Anadyr Peninsula (Russia).

The modern walrus feeds predominantly on mollusks, and uniquely feeds by placing the shell inside its lips and sucking the muscle tissue directly out of the poor little clam: the shell never enters the mouth, and the teeth are not used at all during feeding. Instead, the highly vaulted palate of the walrus permits the muscular tongue to act like a powerful piston as it is retracted. It also allows the walrus to jet out water onto the seafloor to uncover individual mollusks during foraging. The walrus is otherwise unique amongst pinnipeds by routinely mating in the water; unlike many other pinnipeds, the walrus also is flexible when it comes to where it hauls out – it can haul out on icepack or rocky beaches. Many other pinnipeds only haul out on a certain substrate, whether its sand (e.g. NZ sea lion, elephant seals), rocky shore (NZ fur seal), or ice (most arctic and Antarctic true seals). Most famous of all, however, are the spectacular tusks of walruses – greatly enlarged upper canines that are so long they protrude eternally from the animal’s mouth. What did tusks evolve for? A few studies have advanced various hypotheses, and the evolution of tusks will be considered in a later post in this series.

A somewhat outdated hypothesis of walrus relationships (from Barnes et al., 1985) - however, this figure is still informative, and is one of the only cladograms labeled with anatomical illustrations. I'm currently working on enough skull illustrations to make a modern version with an updated phylogeny. Notably absent from this phenogram are true seals, which were left out in the spirit of pinniped diphyly.

The most up-to-date hypothesis of walrus phylogeny, showing many of the interrelationships amongst the Odobenidae. For the purpose of this blog post, note the basal position of Prototaria, Proneotherium, Neotherium, and Kamtschatarctos. From Boessenecker and Churchill (2013).

Lastly, the phylogenetic relationships of walruses have proved contentious. Although the relationships within the family Odobenidae are fairly well resolved (compare the cladistic results of Deméré, 1994, Deméré and Berta, 2001, Kohno, 2006, and Boessenecker and Churchill, 2013), the relationships of the family to other pinniped clades has been a major point of debate, if not a source of ideological schism within pinniped paleontology (an admittedly small subdiscipline). Traditionally, walruses have been placed into a clade called Otarioidea including all pinniped groups except for the Phocidae; Otarioidea (or a much more taxonomically inclusive Otariidae of some authors, e.g. Mitchell and Barnes) would include the Otariidae, Odobenidae, Desmatophocidae, and the “enaliarctines” (early primitive pinnipeds). This traditional view has generally been based on non-cladistic interpretations of morphological evidence. Viewpoints typically endorsing monophyly of Otarioidea also consider the pinnipeds to be diphyletic, with phocids evolving from an as-yet unidentified mustelid ancestor and otarioids evolving from a bear-like ancestor. A more recent interpretation based on robust cladistic work (Berta and Wyss, 1994) endorses a phylogeny of pinnipeds that is fundamentally different in three ways: 1) pinnipeds are indeed monophyletic, 2) extant phocid seals and extinct desmatophocids (e.g. Allodesmus) form a clade, the Phocoidea, and 3) the walruses (Odobenidae) are sister to the Phocoidea, forming the clade Phocomorpha – including walruses, true seals, and desmatophocids. The Phocomorpha hypothesis is superior to the Otarioidea hypothesis by virtue of actually having cladistic evidence that supports it. Further complicating these matters is the fact that modern molecular studies – virtually all of them – unilaterally demonstrate that pinnipeds are a monophyletic group, typically with 100% branch support in every study. However, virtually all of these molecular studies also indicate – again with robust support – that otariids and odobenids form a monophyletic group to the exclusion of phocids. Ironically, for once, the molecular work doesn’t really go at odds with the morphological evidence so much as it actually provides sort of a satisfying compromise between two extremes. Regardless, the molecular hypotheses for relationships within pinnipeds are still lacking support from morphological evidence. More on this will be discussed later.

The rest of this post will focus on sea lion-like pinnipeds now known to be walruses, but they lack tusks and were small in stature and did not live on ice; how do we know they're walruses? A few unique features unite all fossil and modern walruses: an antorbital process of the rostrum composed of both frontal and maxilla, a thickened "pterygoid strut" at the posterior end of the palate, an internal ridge called the tentorium overlapping the inner ear bone, lingual cusps on the upper anterior premolar teeth, and a triple rooted upper molar (a reversal to the primitive condition in terrestrial arctoids, whereas in enaliarctines the tooth is double rooted; both dental features are lost in later odobenids). A few postcranial features  (mostly humerus, radius, the first metacarpal, and a wrist bone called the scapholunar), also unite all walruses (some early walruses are not yet known from well preserved postcranial bones).

One of the earliest discovered fossils of a stem walrus: the syntype astragalus of
Neotherium mirum, described by Kellogg (1931) from the middle Miocene Sharktooth Hill Bonebed.

The earliest walruses

The earliest known walruses evaded identification for nearly forty years. Part of the problem was that prior to the 1970’s, nobody knew what a primitive pinniped looked like, and the scarcity of early molecular work meant that nobody knew where pinnipeds fit within Carnivora, further meaning that nobody knew what a primitive pinniped should look like. Although now known to be an early walrus, the pinniped Neotherium mirum was named in 1931 by Remington Kellogg from the Sharktooth Hill Bonebed based on a paltry handful of non-associated ankle bones. Kellogg tentatively considered it to represent an otariid pinniped (and judging from the size of the postcranial bones accurately estimated its size to be somewhat smaller than an extant adult female California sea lion), but even later workers (e.g. Mitchell, 1961) considered the identity of Neotherium to be tenuously known at best. In 1968, Ed Mitchell described the new genus Imagotaria from the late Miocene Monterey/Sisquoc Formation of Santa Barbara County, which at the time he considered to be an ancestral sea lion closely related to the gigantic pinniped Pontolis magnus. Pontolis had been discovered at about the turn of the century in the Empire Formation near Coos Bay, Oregon, and until the 1990’s was only known from a gigantic incomplete braincase.

In 1973, Ed Mitchell and Richard Tedford described the early pinniped Enaliarctos mealsi from the Jewett Sand at Pyramid Hill, a prolific locality near Bakersfield, California (not too far away from the more famous Sharktooth Hill) which has yielded a lot of important marine vertebrate fossils from about the Oligo-Miocene boundary. Enaliarctos mealsi effectively resembles a fur seal with the dentition and other skull features of a terrestrial carnivore. While clearly not a walrus, at least by this point the primitive condition of the pinniped skull was known and could be compared with later fossils.

In 1977, a monograph was published by Charles Repenning and Richard Tedford titled “Otarioid Seals of the Neogene”, one of the most important contributions – if not the most important contribution - in the history of fossil pinniped studies. I affectionately call their paper the “pinniped bible”. In their paper, they described a new fossil walrus that will be discussed in more detail later, Aivukus cedrosensis – and described more skulls, mandibles, and postcranial bones of Imagotaria. These new discoveries indicated that in the past, walruses did not always have tusks and had a more generalized sea lion-like skull and dentition, probably signifying a more generalized ecology. Imagotaria and company will be discussed in more detail in the next post.

The indifferently preserved holotype skull and (somewhat better) mandible of Kamtschatarctos sinelnikovae, from Dubrovo (1981).

The first early walruses to have been described from skulls were not from North America, but rather from the western North Pacific – Kamtschatarctos sinelnikovae, from the middle Miocene of Kamtchatka (Dubrovo, 1981) in eastern Russia (then, the Soviet Union), and Prototaria primigena from the early middle Miocene of Japan (Takeyama and Ozawa, 1984). Neither of these were immediately recognized as walruses, but Barnes (1989) identified that both shared features with Imagotaria and (at the time) undescribed cranial material of Neotherium. Initially, Dubrovo (1981) named a new subfamily, the Kamtschatarctinae, to contain Kamtschatarctos (only) within the family “Enaliarctidae”. The Russian species is known only from a single squashed and incomplete skull with a rather delicate mandible. The most immediate alarm bell about this skull is its size – it’s quite a bit larger than all known enaliarctine material; so far as we know, all described enaliarctines were approximately the size of a harbor seal or so. Dubrovo (1981) drew attention to the root condition, although Barnes (1989) correctly indicated that the rooting was a primitive condition, and that the mandible (and root condition of the dentition) is quite similar to Imagotaria downsi in some regards. Despite being much more similar to Enaliarctos in overall skull morphology than Kamtschatarctos, Takeyama and Ozawa (1984) considered the much better preserved skull of Prototaria to be an early otariid (rather than an enaliarctine) morphologically intermediate between Enaliarctos and the fossil fur seal Thalassoleon. However, Barnes (1989) identified a number of primitive features it shares with undescribed cranial material of Neotherium, and even went so far as to reclassify it as Neotherium primigena.

The holotype skull and partial skeleton of Prototaria primigena, described by Takeyama and Ozawa (1984) from the early middle Miocene of Japan. Unfortunately, only the skull has been described and it is unclear if and when the postcrania will be described.

In 1994, Naoki Kohno described a second species of Prototaria from Japan, and named it Prototaria planicephala, alluding to its relatively flat skull. Both species of Prototaria are relatively tiny – about the size of a modern harbor seal – with relatively short snouts (rostra) and a generalized dentition. Both species are known from the early Middle Miocene of Japan. Kohno (1994) indicated that new skull material of Neotherium demonstrated that Prototaria was in fact a distinct, separate genus, primarily by the shorter rostrum, a more massively constructed zygomatic arch, and a few less interesting differences. Prototaria exhibits at least one feature (synapomorphy) uniting all walruses – a thickened pterygoid strut in the basicranium, a bony strut laterally adjacent to the internal choanae and posterior to the palate; this feature is present in most archaic walruses, differentiating them from all other pinnipeds – and is secondarily lost in later walruses. Other than this single important feature, Prototaria is nearly identical to enaliarctines like Enaliarctos and Pteronarctos, even primitively possessing small supraorbital processes (primitive for carnivorans, reduced in most odobenids, desmatophocids, and phocid seals).

Illustration of the holotype skull of Prototaria planicephala from the early middle Miocene of Japan, from Kohno (1994).

The next significant advance was the publication of skull material of Neotherium mirum and the naming of Proneotherium repenningi, from the middle Miocene Sharktooth Hill Bonebed and the late early-early Middle Miocene Astoria Formation of Oregon (respectively). Proneotherium is known by numerous skulls and a partial postcranial skeleton, and at least one mandible (Kohno et al., 1995; Deméré and Berta, 2001; Boessenecker and Churchill, 2013). Proneotherium has a more or less enaliarctine-like skull and postcranial skeleton, but already has at least one postcranial synapomorphy – a medial process on the calcaneum (the heel bone). Proneotherium also has an expanded pterygoid strut like Prototaria, and has a posterolingual shelf on some of its cheek teeth – a feature not preserved in Prototaria. A feature Morgan Churchill and I found in a referred mandible of Proneotherium which we figured in our paper on Pelagiarctos – is the position of the deepest part of the tooth-bearing part of the mandible (the “horizontal ramus”). In Enaliarctos and Pteronarctos, the deepest part is positioned at the lower molar, which is still shaped as a large carnassial shearing tooth; this is the primitive condition for carnivores. However, in Proneotherium, all later walruses, and modern sea lions and fur seals, the deepest part of the mandible is positioned anteriorly at the canines, giving the impression of a “deep” or “thick” chin. This condition is generally lacking in most modern and fossil true seals and the extinct pinniped Allodesmus, but is present in the other desmatophocid, Desmatophoca. Kohno et al. (1995) described the holotype skull and also designated a paratype skull; Deméré and Berta (2001) referred several additional skulls, including one associated with a partial postcranial skeleton. As an aside, Larry Barnes told me that Proneotherium was a pet name (since it was smaller, older, and thought to be ancestral to Neotherium) for this material used by the late Charles Repenning during the 1980’s; Barnes (in Kohno et al., 1995) decided to use the name and named the species after Repenning (a fitting honor for Rep). I never met Repenning unfortunately, as he was murdered in his home in 2005, the year I started marine mammal paleontology research.

Well-preserved skulls of Proneotherium repenningi from the early middle Miocene Astoria Formation of Oregon described by Demere and Berta (2001).

The last of the early small-bodied odobenids, Neotherium, is known widely from the Sharktooth Hill Bonebed. It was first described by Kellogg (1931) based upon a handful of non-associated cranial elements. Subsequent workers referred various bits including a humerus (Mitchell, 1961), radius (Repenning and Tedford, 1977), a mandible (Barnes, 1988) and finally a complete skull (Kohno et al., 1995). Repenning and Tedford (1977) noted that material of Neotherium effectively looked like miniature bones of Imagotaria; because only one small bodied walrus is known from the Sharktooth Hill Bonebed, isolated bones matching the size are referable to the species if they look similar to Imagotaria. On the other hand, Imagotaria is known from numerous specimens with associated craniodental and postcranial elements, whereas all material of Neotherium from the bonebed is isolated and not associated. Neotherium is notably distinct from Proneotherium, Prototaria, and enaliarctines in its complete lack of supraorbital processes – the first walrus to have lost these bumps above the orbits.

Comparison of the skulls of Proneotherium repenningi (left), Neotherium mirum (middle), and Imagotaria downsi (right).

In summary – during the early and middle Miocene, we have the earliest walruses evolve from enaliarctines. These early diverging walruses were small, probably about the same size as a harbor seal – or a small sea lion in the case of Neotherium. The dentition of these walruses was barely different from enaliarctines, although they lacked the dedicated carnassial shearing teeth of enaliarctines. Mitchell and Tedford (1973) suggested that Enaliarctos may have needed to return to land in order to chew, given that it was still using a primitive shearing dentition (some in-preparation work by Morgan Churchill will be weighing in on this in more detail). If this assertion is true, then the earliest walruses were certainly already pierce or raptorial feeders – biting prey items and swallowing them whole. Importantly, the palates of these early walruses were relatively flat – indicating that suction of prey into the mouth was not yet an important aspect of their feeding ecology (similar to most true seals and otariids).

A well-preserved skull of Neotherium mirum from the middle Miocene Sharktooth Hill Bonebed described by Kohno et al. (1995).

One curious trend seen in early walruses is the process of “molarization”. In these early walruses, the anterior premolars begin to look more and more like the molars, developing a thickened lingual cingulum (lingual = tongue side of the tooth, and cingulum is a ridge of enamel along the base of the crown) and even developing a thickened posterior root (in enaliarctines, anterior premolars have two skinny, cylindrical roots). Usually a transversely thickened root suggests that two roots have been fused into one; some of the upper teeth (notably the upper molar and upper fourth premolar in caniform carnivores) are primitively triple-rooted, with one anterior root and two posterior roots; one way to fuse up these roots during the process of tooth simplification is to fuse the two posterior roots together. This leads to a tooth that is double-rooted, but has a small cylindrical anterior root and a much wider posterior root; this condition is then typically reduced further into two cylindrical roots (as in most modern true seals), and eventually into a single fused root (as in the modern walrus and extant fur seals and sea lions). Tooth rooting can be a good “barometer” of how primitive or derived a particular fossil pinniped is, as the dentition has been simplified in all groups from the ancestral enaliarctine condition – and single-rooted teeth have evolved no fewer than six or seven times amongst pinnipeds (Boessenecker, 2011). Early walruses, on the other hand, seemed to be doing the opposite: the anterior premolars were being increased in size and complexity, adding a thickened lingual cingulum and even developing small cusps on it. It’s not really clear why this happened, or what the advantage was – the general rule of dental evolution in pinnipeds (and marine mammals in general) is tooth simplification. Only a few groups of marine mammals ever added any cusps to their teeth: basilosaurids (and some toothed mysticetes) added a bunch of cusps to their cheek teeth, as did leopard and crabeater seals. Other marine mammals such as Odobenocetops, narwhals (Monodon), and later walruses increased the size of some teeth and developed tusks, but I imagine that’s something much more easily governed by rampant sexual selection (again, more on that in a later post).

Line drawings of skulls in lateral view, including Enaliarctos mealsi (upper left) and Prototaria, Proneotherium, Neotherium, and Kamtschatarctos.

Postcranial bones have only really been published for Proneotherium (Deméré and Berta, 2001), although a handful of comparable elements have been published for Neotherium; they do not strongly differ, and functional statements/interpretations based on Proneotherium are likely to apply equally to Neotherium. The preserved hindlimb of Proneotherium shows it had various hallmark features of modern pinnipeds (Deméré and Berta, 2001), including a short femur and long tibia, long and robust lateral and medial digits (digits I and V) of the hindflipper with shorter intermediate digits (e.g. digits II, III, and IV). These two osteological features indicate that Proneotherium – and likely most other early walruses – already had a permanently flexed knee and also fan-shaped symmetrical hindflippers. However, Proneotherium primitively retains a pit on the head of the femur for the teres ligament (a ligament that keeps the head of the femur in the hip socket, missing in modern pinnipeds – both the ligament and the pit), and also primitively retains a lesser trochanter (a bump below the head of the femur, missing in many modern pinnipeds). Lastly, the ankle of Proneotherium is rigidly constructed indicating a substantial amount of terrestrial locomotion, as in modern otariids and terrestrial carnivores; the ankle of phocid seals is constructed as a loose ball-and-socket joint, and odobenine walruses have an intermediate but nonetheless loose ankle joint. This rigid ankle would have constrained movement of the hindflipper into flexion and extension and reducing rotation of the ankle – a retained adaptation for terrestrial walking.

This summary has highlighted a primitive pinniped that doesn’t really recall a mental image that looks anything like a walrus. Why is that? Pinnipeds began to diversify shortly after their invasion of the marine realm, and walruses are the earliest modern family of pinniped for which we can assign any fossils (specifically, Prototaria from Japan). The oldest known true seals are a bit younger (~15 Ma, Leptophoca from the Calvert Formation of Maryland; although the fragmentary Afrophoca is somewhat older, ~19 Ma), and the oldest otariids are a lot younger (~8-10 Ma, Pithanotaria from the Monterey Formation and Santa Margarita Sandstone of California). Although being relatively similar to primitive enaliarctines in most respects, these early walruses have just enough skull features to pull them closer to the modern walrus in cladistic analyses. Sometimes these early diverging walruses have been assigned to the subfamily “Imagotariinae” – but the “Imagotariinae” is not monophyletic (because it includes only primitive species and none of the later odobenids). I’ve only outlined the small-bodied early “imagotariines” here; the next post will cover the larger imagotariines like Imagotaria, Pelagiarctos, and Pseudotaria. At least three more posts will follow after that: a post on the bizarre dusignathine walruses, odobenine walruses and their evolutionary biogeography, and another post on the evolution of tusks.


Barnes, L.G. 1988. A new fossil pinniped (Mammalia: Otariidae) from the middle Miocene Sharktooth Hill Bonebed, California. Contributions in Science 396:1-11

Barnes LG, Domning DP, Ray CE. 1985. Status of studies on fossil marine mammals. Marine Mammal Science 1:15-53.

Boessenecker, R.W. 2011. New records of the fur seal Callorhinus (Carnivora: Otariidae) from the Plio-Pleistocene Rio Dell Formation of Northern California and comments on otariid dental evolution. Journal of Vertebrate Paleontology 31(2):454-467.

Boessenecker, R.W., and M. Churchill. 2013. A Reevaluation of the Morphology, Paleoecology, and Phylogenetic Relationships of the Enigmatic Walrus Pelagiarctos. PLoS One 8(1):e5411

Deméré. 1994. The Family Odobenidae: A phylogenetic analysis of fossil and living taxa. Proceedings of the San Diego Society of Natural History 29:99-123

Deméré, T.A., and A. Berta. 2001. A re-evaluation of Proneotherium repenningi from the middle Miocene Astoria Formation of Oregon and its position as a basal odobenid (Pinnipedia: Mammalia). Journal of Vertebrate Paleontology 21(2): 279-310.

Dubrovo, I.A. 1981. A new subfamily of fossil seals (Pinnipedia, Kamtschatarctinae subfam. nov.). Doklady Earth Science Sections 256:202-206

Kellogg, R. 1931. Pelagic mammals of the Temblor Formation of the Kern River region, California. Proceedings of the California Academy of Science 19(12):217-397.

Kohno, N. 1994. A new miocene pinniped in the genus Prototaria (Carnivora: Odobenidae) from the Moniwa Formation, Miyagi, Japan. Journal of Vertebrate Paleontology 14(3):414-426

Kohno, N. 2006. A new Miocene odobenid (Mammalia: Carnivora) from Hokkaido, Japan, and its implications for odobenid phylogeny. Journal of Vertebrate Paleontology 26(2):411-421

Kohno, N., L. G. Barnes, and K. Hirota. 1995. Miocene fossil pinnipeds of the genera Prototaria and Neotherium (Carnivora; Otariidae; Imagotariinae) in the North Pacific Ocean: Evolution, relationships and distribution. The Island Arc 3:285-308

Mitchell, E.D. 1961. A new walrus from the imperial Pliocene of Southern California: with notes on odobenid and otariid humeri. Los Angeles County Museum Contributions in Science 44:1-28

Mitchell, E.D. 1968. The Mio-Pliocene pinniped Imagotaria. Journal of the Fisheries Research Board of Canada 25(9):1843-1900.

Mitchell, E.D. and R. H. Tedford. 1973. The Enaliarctinae: A new group of extinct aquatic Carnivora and a consideration of the origin of the otariidae. Bulletin of the American Museum of Natural History 151(3):203-284

Repenning, C.A. and R. H. Tedford. 1977. Otarioid seals of the Neogene. Geological Survey Professional Paper 992:1-93

Takeyama, K. and T. Ozawa. 1984. A new Miocene otarioid seal from Japan. Proceedings of the Japan Academy Series B Physical and Biological Sciences 40(3):36-39

Tuesday, August 19, 2014

Farewell to Mike Gottfried - annual NZ research visit

Today is visiting paleoichthyologist Dr. Mike Gottfried's last day on his research visit to our department. Mike comes down to New Zealand once a year during the southern winter to collaborate on various research projects with Ewan. Prior projects have resulted in the description of an associated dentition and vertebral column of the giant shark Carcharocles angustidens, the giant moonfish Megalampris keyesi, and the billfish Aglyptorhynchus hakataramea.

Mike's current visit has been to identify Paleogene sharks and fish collected during the Lost Mammals of Zealandia project, in addition to describing a new genus and species of Cretaceous-Paleogene tarpon from the Chatham Islands (in tray in photograph). It's always a pleasure to have Mike down here, least of which because it's always nice to commiserate with another Yankee, but also nice to have someone to talk about fossil sharks. I'll be graduated before Mike's next visit to New Zealand, so farewell Mike! Have fun stateside.

Sunday, August 17, 2014

New publication: phylogenetic relationships of fur seals and sea lions (Otariidae)

Last week saw publication of a new study by Morgan Churchill, Mark Clementz, and myself, which presents a new cladistic analysis of the pinniped family Otariidae (Morphobank account/matrix available HERE) - known informally as fur seals and sea lions. I've been fascinated with fossil otariids since I started research on a specimen of the Pliocene dwarf fur seal Callorhinus gilmorei from the Rio Dell Formation in Northern California. This collaboration has been about two years in the making, and began shortly after we started work on the Pelagiarctos study published last year in PLOS One.

There are about 13-16 species of modern otariids in 7 (or 8) genera - 9 of which are fur seals in the genera Arctocephalus (some may be Arctophoca) and Callorhinus. Fur seals are generally smaller-bodied than sea lions, and are primitively characterized by retaining dense underfur - whereas sea lions have a thicker blubber layer, only possess hair (as opposed to underfur) and are generally much larger. Modern otariids are externally very similar, and it can be very difficult to tell them apart. Fur seals (with the exception of the Northern Fur Seal Callorhinus ursinus which has a distinctive snout shape) in particular are nearly impossible to tell apart externally, and identifications of osteological remains are often made based upon the geographic location as few geographically overlap with one another. Different species of Arctocephalus are nearly identical in skull morphology - however, sea lions are more morphologically distinct from one another. For example, California sea lions (Zalophus californianus) have a huge sagittal crest but an otherwise Arctocephalus-like skull, and the Steller's sea lion (Eumetopias jubatus) and New Zealand sea lion (Phocarctos hookeri) have a "domed" forehead. The Australian sea lion (Neophoca cinerea) has an unusually robust intertemporal region, while the South American sea lion (Otaria byronia) has a very elongate palate, procumbent upper third incisors and canines, and rugose tubercles on the side of the braincase (an elongate palate is also present in Phocarctos).

Relative to other pinnipeds (walruses, Odobenidae, and true seals, Phocidae), otariids primitively possess external ear pinnae (the type genus Otaria comes from the greek Otarion, meaning little ear, the most adorable name possible for such an intimidating monster as the south american sea lion), and can rotate their hindflippers forward and walk when on land - walruses are capable of this type of terrestrial locomotion as well, but true seals have an ankle that is more extremely adapted for swimming and can no longer rotate forward. The result is that their feet are permanently extended posteriorly - the same motion your ankle makes when standing on on your tiptoes. The long wing-like forelimbs of otariids permits underwater flying, in a manner reminiscent of bird flight.

Pinniped phylogeny of Barnes et al. (1985). Note that true seals are notably lacking from this hypothesis: most studies of pinniped evolution prior to the late 1980's were done under the now-outdated paradigm of pinniped diphyly.

Modern hypotheses for fur seal and sea lion relationships began under the assumption of pinniped diphyly, and this idea is pervasive in practically all papers on pinniped evolution published between 1960 and 1987 - while the idea has mostly faded away, a few paleontologists adhere to the idea. Effectively, pinniped diphyly maintains that otariids, odobenids, and the extinct desmatophocid seals form a natural group (the Otarioidea) that evolved from bear-like ancestors (Ursidae) and that true seals independently evolved from the weasel family (Mustelidae). This hypothesis was first challenged in 1987 when Andre Wyss identified a number of basicranial features linking walruses with true seals - suggesting not only that pinnipeds were diphyletic, but also that Otarioidea may not be monophyletic. Pinniped monophyly has been corroborated by many subsequent morphological studies and virtually every single molecular analysis of carnivoran phylogeny ever published, whereas pinniped diphyly has never been robustly supported by a single cladistic analysis of morphological data (in other words, proponents of pinniped diphyly have relied upon hand drawn cladograms).

Interrelationships of otariids were generally not investigated much prior to the advent of cladistics, with the exception that otariids were assumed to contain two natural groups: the fur seals (Arctocephalinae: Arctocephalus/Arctophoca + Callorhinus) and the sea lions (Otariinae: Eumetopias, Neophoca, Otaria, Phocarctos, Zalophus). The first cladistic analysis of otariid relationships conducted by Berta and Demere (1986) initially supported the monophyly of these two subfamilies, but has been subsequently challenged by most molecular analyses which indicate that both subfamilies are paraphyletic, with large body size and dense underfur being lost and gained several times.

Some molecular cladistic results from prior studies.

Aside from the first study by Berta and Demere (1986), only two following studies published morphological analyses of the otariidae: a paper by Demere and Berta (2005) included a cladogram from a separate unpublished study, and a fully published cladistic analysis published by Barnes et al. (2006) for the newly described fossil sea lion Proterozetes. Neither of these studies used more than 45 characters, which is more than some other papers I've read, but Morgan and I felt like more could be done. So, we surveyed the literature for additional characters, including some from published studies on phocid phylogeny which were just as useful to look at morphological variation within otariids, in addition to brainstorming totally new characters nobody else had thought of yet.

One of the problems facing us is that for some features, there is quite a lot of variation within a single species - for example, in most mammals there is a healthy amount of variation within a species. Think about how different everyone looks on your next bus or subway ride - the same applies to other mammals. Dental variation is remarkably common, with many individuals having double rooted teeth versus single rooted in others, or have more strongly developed cusps or ridges called cingula. When you code characters for a cladistic analysis, you have different character states summarized by numbers. An example would be character #X - labial cingulum on upper postcanine teeth (in English, a small ridge around the base of the crown on the cheek side of the tooth): 0- present. 1- absent. It's present in primitive pinnipeds like Enaliarctos, but absent in most modern pinnipeds - except some sea lions, where it has secondarily evolved (called a reversal). The problem is that for some species, some individuals have lingual cingula and others do not - this sort of variation is called a polymorphism, and it means that species is coded for both character states (01 in the cladistic matrix). When a 01 is coded, the program effectively treats it as a big "?" and the character is uninformative for that taxon. A way to get around this and still harness the usefulness of that polymorphic condition (because in many cases it represents the incipient development of the derived condition) is to introduce an intermediate "polymorphic" character state (0=present, 1=polymorphic, 2=absent) and run the character as an ordered (or additive) character (in other words, the program treats the character states as progressing from one to another, rather than unordered, the typical manner in which vertebrate morphologists treat cladistic characters).

We were also careful to avoid ambiguous character definitions, which are prevalent in many older studies. Whenever possible, we used ratios to define different states (e.g. long, >80% of the length of some other measurement). Vaguely defined characters basically prevent future researchers from replicating your analysis if they have no damn clue what you were talking about. Another problem prevalent in pinnipeds is sexual dimorphism: males are much larger than females, a life history trait that carries over into their skeletons. The skulls and mandibles of males look quite a bit different than females - female skulls are more generalized and gracile and often lack some of the structural peculiarities that permit identification of skulls, to the point where most female otariids look extremely similar. To circumvent this problem, whenever possible we only coded from adult male specimens. I have no idea how to run molecular analyses, but Morgan's done plenty of it, so he additionally ran some molecular analyses and a combined (morphology + molecules) analysis.

Morphology-based phylogenetic results from our new paper.

As for our results? Well, we found that some differences in sampling and search method produced a few minor changes in topology. Our morphology-only analyses tended to support sea lion (Otariinae) monophyly, and also supported fur seal (Arctocephalinae) paraphyly. Our molecular and combined analyses, however, showed that both groups are likely paraphyletic. One of the only results that was universal among these different analyses was a Eumetopias + Zalophus clade, which is supported by most previous analyses of molecular data (we also confirmed this for morphology, which is a good step forward). Similarly, we also consistently recovered a sister taxon relationship between the Pleistocene sea lion Proterozetes and the extant Steller's sea lion Eumetopias, to which Zalophus was sister, a clade we gave the unimaginative name "Northern sea lion clade". I have for a long while thought that Proterozetes was an unnecessary name, and that it should be recombined as Eumetopias ulysses, although Proterozetes does have a couple of Zalophus-like features, such as a higher sagittal crest and a more gracile rostrum and a skull that is slightly proportionally shorter than Eumetopias, suggesting that Eumetopias evolved as a sort of "mega" California sea lion.

Most North Pacific fossil fur seals (Thalassoleon mexicanus, macnallyae, and inouei) were consistently placed on the otariid stem, but without good support. The extant Northern fur seal, Callorhinus ursinus, was typically the earliest diverging extant otariid; no sister group relationship with Callorhinus gilmorei was supported, although some of the key features of Callorhinus ursinus (dorsally inflated maxilla, higher facial angle) are not yet known for published specimens of Callorhinus gilmorei and we were unable to code for these characters. Discovery of skulls of Callorhinus gilmorei can probably alleviate this problem - stay tuned. The fossil fur seal Hydrarctos lomasiensis from Peru, on the other hand, consistently plotted out in the sea lion-Arctocephalus/Arctophoca clade. The last significant fossil otariid, Neophoca palatina from the Pleistocene of New Zealand, kinda came out all over the place: it's a nice skull (what's left of it - more on that in the future, so again, stay tuned) but it critically lacks the tip of the rostrum and the dentition, and has no other elements.

Why were our results for fossil otariids so... disappointing? It's largely due to the fact that there isn't much variation between even modern otariid species, and if a fossil has anything other than a nearly complete skull, some of the more obscure peculiarities necessary for good phylogenetic resolution are going to be absent and not codable. Furthermore, fossil otariids are relatively derived and we don't have any examples of otariids that have plesimorphic morphology intermediate between something like a fur seal and an early enaliarctine pinnipedimorph. We know they're pinnipeds, and we know they evolved from an enaliarctine-like ancestor, but the transitional fossils just don't exist (yet... stay tuned, again!). The otariid fossil record is also temporally shallow - the oldest known otariid is a Pithanotaria-like mandible from the late Miocene Aoki Formation of Japan (12.5-11.8 Ma; Kohno et al. 2007). In contrast, fossil phocids go back to 19 Ma (Afrophoca), fossil odobenids are known from about 16-17.5 Ma (Prototaria, Proneotherium, Pelagiarctos), and desmatophocids go back to about 19 Ma as well (Desmatophoca brachycephala). Difficulty for modern otariids results from a general lack of ecological specialization, a relatively recent diversification (see below) and frequent hybridization. Furthermore, some species - particularly Artcophoca phillippii, A. tropicalis, and A. gazella, are currently rare and distributed only on remote islands, and large accessible collections of these species were not really available for our study.

Phylogenetic relationships can be interesting in and of themselves, but after hundreds of hours staring at a big matrix of 0s and 1s you may be attempted to slit your wrists just to see some color - cladistics is a great tool, and while a lot of people enjoy doing nothing else, it's healthy to mix it up a little bit and use those cladistic results for addressing something more interesting. One question we addressed was biogeography - the fossil record of otariids is pretty craptacular, and various biogeographic hypotheses have been advanced purely on molecular results. That's fine, and often necessary, but even a crappy fossil record is a great opportunity to constrain or spot check hypotheses - since fossils invariably reflect the presence (or in some cases, absence) of a particular taxon in a particular region (ocean basins in our case). Otariids have generally thought to have had a North Pacific origin, thanks due in part to the fossil record (Pithanotaria, Thalassoleon) and the earliest diverging extant otariid - Callorhinus - still lives here (and has never left). However, only about 1/3 of extant otariid species live here today, and most inhabit the southern hemisphere. Previous studies suggested a Plio-Pleistocene dispersal to the southern hemisphere. Our results - an ancestral character state analysis of biogeography - show a North Pacific origin for otariids (unsurprisingly), with the Australian sea lion, Neophoca, and the monophyletic southern otariid clade (Phocarctos + Otaria + Arctocephalus/Artcophoca) independently dispersing to the southern hemisphere. The fossil Hydrarctos, which is apparently as old as 6.6 Ma or so (and as young as 3.9 Ma), sets a minimum and maximum date for this dispersal. A single femur identified as Arctocephalus from South Africa about 3-5 Ma also sets some constraints for the dispersal.

Further constraint may be included when sea surface temperatures tolerated by extant otariids are plotted onto the phylogeny. We reconstructed the ancestral water temperature toleration for the southern otariid clade as 22-20 degrees celsius at the most: for the uninitiated, warm water is an effective barrier towards marine mammal dispersal, and is generally more important than cold water for restricting marine mammal migration/dispersal (sea and pack ice can be another). Many modern species cannot cross the equator, largely owing to the absence of abundant food. In cold, nutrient-rich cold temperate waters of the eastern Pacific, the ocean teems with life and marine mammals are locally abundant. To put in a plug for another paper, I discussed this quite a bit in my recent paper in Geodiversitas and proposed that the equatorial warm water barrier (in concert with the unopened Bering strait and the recently closed Central American seaway) permitted a highly distinct, provincial marine mammal fauna to evolve in the eastern North Pacific (Boessenecker, 2013). Two periods in the late Neogene saw equatorial waters become cool enough to permit temperate/cold temperate otariids cross from North to South: late Pliocene global cooling beginning about 3 Ma, and an older period of cooler water and increased upwelling took place about 6-7 Ma. From 3-5 Ma the equatorial Pacific was relatively warm and characterized by permanent El Nino conditions, and warmer than the reconstructed temperature tolerance of the southern otariid clade. Prior to 7 Ma, the equatorial waters were relatively warm and would have been an effective barrier to otariid dispersal. Coincidentally, a separate study (Yonezawa et al. 2009 - to date, the most convincing molecular study of otariids in my opinion) found a ~7 Ma molecular date for the diversification of the southern otariid clade. The fossil record indicates that otariids were already present in the southern hemisphere before the 3 Ma initiation of glacial-related global sea surface cooling, and the combination of the fossil record, molecular date, and temperature data strongly suggest a southern dispersal around 6-7 Ma. Certainly, the densely sampled Pisco Formation of Peru has yielded no otariids older than about 6.6 Ma (and has yielded an otherwise well-sampled and rich marine mammal fauna from multiple stratigraphic horizons), corroborating this estimate.

What future work remains to be done? More work on some of the more obscure southern hemisphere fur seals is necessary (and the Guadalupe fur seal, for that matter). Better molecular sampling of otariids, and a larger osteological sample size of some species is necessary. We of course need more fossil otariids - more digging in non-Sharktooth Hill middle Miocene deposits! Otariids apparently just weren't in the Temblor Sea, and early otariids may yet be hiding in middle Miocene rocks from the California and Oregon coast, and Japan.

For our morphobank account, CLICK HERE.


Barnes LG, Domning DP, Ray CE. 1985. Status of studies on fossil marine mammals. Marine Mammal Science 1:15-53.

Barnes LG, Ray CE, Koretsky IA. 2006. A new Pliocene sea lion Proterozetes ulysses (Mammalia: Otariidae) from Oregon, U.S.A. In: Csiki Z, ed. Mesozoic and Cenozoic vertebrates and paleoenvironments: tributes to the career of Prof. Dan Grigorescu. Bucharest: Ars Docendi, 57–77.

Berta A, Deméré TA. 1986. Callorhinus gilmorei n. sp., (Carnivora: Otariidae) from the San Diego Formation (Blancan) and its implications for otariid phylogeny. Transactions of the San Diego Society of Natural History 21: 111–126.

Boessenecker RW. 2011. New records of the fur seal Callorhinus (Carnivora: Otariidae) from the Plio-Pleistocene Rio Dell Formation of Northern California and comments on otariid dental evolution. Journal of Vertebrate Paleontology 31: 454–467.

Boessenecker RW. 2013. A new marine vertebrate assemblage from the Late Neogene Purisima Formation in Central California, part II: pinnipeds and cetaceans. Geodiversitas 35: 815-940.

Churchill, M., Boessenecker, R.W., and Clementz, M.T. 2014. Colonization of the Southern Hemisphere by fur seals and sea lions (Carnivora: Otariidae) revealed by combined evidence phylogenetic and Bayesian biogeographical analysis. Zoological Journal of the Linnean Society. In press, online early: onlinelibrary.wiley.com/doi/10.1111/zoj.12163/abstract
Deméré TA, Berta A. 2005. New skeletal material of Thalassoleon (Otariidae: Pinnipedia) from the Late Miocene-Early Pliocene (Hemphillian) of California. Bulletin of the Florida Museum of Natural History 45: 379–411.

Kohno, N., Koike, H. and Narita, K., 2007: Outline of fossil marine mammals from the Middle Miocene Bessho and Aoki Formations, Nagano Prefecture, Japan. Research Report of the Shinshushinmachi Fossil Museum 10: 145.

Yonezawa T, Kohno N, Hasegawa M. 2009. The monophyletic origin of sea lions and fur seals (Carnivora: Otariidae) in the Southern Hemisphere. Gene 441: 89–99.

Thursday, August 14, 2014

Holotype worship and the Hypodigm

I thought a short essay on the treatment of holotypes would be worthwhile. In zoological sciences, many of us are involved in describing and naming new species - in order to maintain taxonomic stability, a type specimen must be designated in a new publication naming a new species. In plain english, the type specimen - also known as a holotype - is the specimen demonstrating the physical evidence for which a new species is named upon. Often when a new species is discovered, researchers will leap to name it - so often, we're stuck with a species named upon a single specimen. It happens frequently in paleontology; finding good fossils is (often) more difficult and more dependent upon sheer luck than going out and finding a second specimen of a newly discovered modern species. As a result, much of the vertebrate fossil record is composed of "singletons" - fossil species represented by single specimens. This problematic nature of the vertebrate fossil record is a favored talking point of young earth creationists, and has also unfortunately contributed to the bizarre opinion amongst some radical cladists that ancestor-descendant relationships are impossible to determine in the fossil record. Radical ideas by folks such as Nature editor Henry Gee come to mind, who rejects all non-cladistic methods in paleontology as being unscientific - an easy position to take if used to the fragmentary vertebrate record of singletons, but difficult to maintain in the face of the enormous and densely sampled record of fossil invertebrates (mollusks and foraminifera come to mind, in which non-cladistic methods can identify speciation events and bouts of anagenesis in vertical successions of fossil assemblages).

The typically fragmentary nature of the vertebrate fossil record, and dealing primarily with singletons, can lead one astray. Subdisciplines divorced from extant relatives and flooded with researchers who do not really look at modern species to get an idea of morphological variation  - dinosaur paleontology comes to mind - may be dominated by an overabundance of taxonomic "splitters" (disclaimer: I have many friends who are dinosaur paleontologists and have a rather sober idea of morphological variation). For the uninitiated, splitters are researchers who tend to name more species than is probably likely; the opposite are "lumpers", who tend to lump species together into a more reasonable framework of fewer names. Many in biology prefer to use a third but unnamed category for the middle ground - I do not, as I consider the "lumper" category the middle ground, and "extreme lumpers" to be on the other end. One marine mammal related example of an extreme lumper is work by Caretto (1970) who lumped all known fossil balaenopterids into a single subspecies, including fossils now known to likely represent several genera. Most "lumpers" I know tend to use morphological variation in related extant species as a tool for interpreting species-level identifications/naming in the fossil record, which sounds reasonable ("eminently sensible" as my adviser would say) - and so I consider anyone reasonably taking a middle ground approach to fossil identification/naming a lumper (versus an extreme lumper).

Many smaller subdisciplines dominated by just a handful of researchers working more or less "unopposed" (i.e. without professional rivals to rigorously dispute work) may be plagued by splitting until some young turk who's spent more time playing with modern skulls comes along and rewrites everything - this has happened time and again in mammalian paleontology. I won't use any examples close to home as many of those researchers involved are still extant, so this discussion is largely going to consist of hypotheticals.

If you spend too much time looking at a relatively small group of fossils - and don't bother looking at modern specimens of extant relatives to take a stab at what sort of range of morphological variation you ought to expect - it's easy to fall into the trap of "typology". I don't necessarily mean the reliance upon type specimens (although I'll eventually get back to that), and the definition of typology is generally given as "a classification according to general type, especially in archaeology, psychology, or the social sciences." In paleontology, typology is a style of thinking in which every fossil species conforms to a different morphological/anatomical "type" (NOT to be confused with the similarly vaguely defined "kind" from young earth creationism). In other words, it should be relatively easy to identify two fossils (or, alternatively, living individuals) of the same species because according to typological thinking, they should look close to identical. For over a century, this was the founding principle of paleontology in practice: if you find something that looks a little different, it's a new species. Done. That's partially why folks like Cope, Marsh, and Leidy published so many damn papers.

The problem is, and this is a concept well known to most paleontologists - biological entities don't give a shit what you think about them. Domesticated animals and humans are some of the more extreme examples - all breeds of domesticated dogs belong to Canis familiaris and can healthily interbreed, but if the entire species was extinct and all we had were skeletons (no ancient DNA), paleontologists would readily name the skulls of a doberman and a chihuahua as different species. With humans, it's a similar case: obviously we know all extant humans can interbreed, but there is a fair amount of morphological diversity, and the human mind is hard wired to recognize familiar faces and as a result exaggerate differences between different populations of humans. Someone who is familiar with other primates would readily note that all humans share much more in common with one another relative to gorillas and chimpanzees, but someone who only looked at human faces and skulls would tend to focus more on the differences rather than the similarities.

Splitting versus lumping continues to be one of the biggest challenges in paleontology - is the new species you've named real, or is it just a morphological extreme? Or is it the opposite gender in a species that is sexually dimorphic? A recent paper just proposed that the Flores hominin - the "Hobbit", Homo floresiensis - is actually just a Homo sapiens with Down's Syndrome. As more and more paleontologists leave dark dusty fossil collections and dabble in neontology, variation is becoming more and more understood and embraced. In the 19th century, vertebrate zoology and paleontology was figuratively the Wild West (and in the case of Marsh and Cope, quite literally). New species which would later turn out to be junior synonyms were published by the bucketload; reading through Victorian era zoological papers often reeks of taxonomic anarchy, with the proliferation of all sorts of species and genus names no longer in use. In many cases, naturalists genuinely were unaware of some papers and discoveries - some species of modern whales and dolphins were independently named and "discovered" literally dozens of times (from different strandings on different continents) during the late 19th century - that's just one of the many problems facing naturalists in the pre-internet world. Some of the synonymy lists for modern dolphins are astoundingly long.

For those unfamiliar with taxonomy but have continued to read this anyway, one of the most important rules set out by the International Code of Zoological Nomenclature (ICZN) is the rule of priority: the species name published first has taxonomic priority. If you name a second species that turns out to be based on an individual from an already-named species, the earlier published name is used. This also applies to genus names - and can spark "nomenclatural wars" like the Aetogate controversy a few years back. If two researchers investigating the same fossil species, and 1) it is an already described species placed in the wrong genus and a new genus name is needed or 2) both parties have found separate fossils of the same, as yet unnamed species - whoever publishes the new name first "wins", so to speak - all other considerations (ethical or otherwise) are irrelevant according to the ICZN. This can both cause extreme tensions in an otherwise small and close knit discipline, or result in the proliferation of synonymous names published in disappointingly brief and poorly figured papers (sometimes called name grabbing, and is the paleontological equivalent of "saving a seat" for yourself).

Now that the discussion of zoological nomenclature has come full circle, it's time to address the title. When in the business of "splitting" and naming new species - particularly when dealing with a record dominated by singletons - it's sort of a no brainer to focus on differences between holotype specimens. There are other types of types - there are paratypes, if you want to clearly designate some key specimens other than a holotype, there are syntypes or cotypes, where a type series is designated but no holotype is selected. There's also lectotypes, where someone selects a single syntype as a retroactive holotype-like designation, and there's also the concept of a neotype - if a type specimen is lost, a neotype conforming enough to the anatomy of the original may be designated afterwards.

But what happens if you have a fossil record that's... better? Admittedly, many parts of the vertebrate fossil record are still awful - but many subsets of the record are pretty damn excellent. What happens when you find a new fossil you think is the same species, but better preserved than the holotype? Paleontologists call these referred specimens - any specimen possessing some evidence that it represents the same species can be considered a referred specimen (e.g. you refer the specimen to a particular taxon). Referred specimens are of immense importance because they can provide 1) information on the anatomy of parts not preserved in the holotype and provide 2) information on anatomical variation for parts that overlap with the holotype. We already know that modern species display an impressive amount of variation, and paleontology is science after all, so in theory we should be using as much evidence as possible to improve our understanding of extinct species in the fossil record.

 Some researchers, however, prefer to focus only on holotypes. You can easily lead yourself into a trap where you assume that the holotype specimen either 1) faithfully represents the morphological "type" of a species or 2) faithfully represents the morphological midpoint of a particular species (and is thus not an outlier in terms of its morphology). Both of these are actually pretty terrible assumptions to make, because in the absence of additional specimens, there's no objective way to defend (or even evaluate) either assumption. I've been told to "stick to holotypes" before, and have heard some Researcher A casually dismiss the careful work of Researcher B who referred additional specimens to a species originally named by Researcher A - and the reasoning was that they were dealing with non-types! I've even had some curators and collections managers give me puzzled looks when I asked to see some obscure referred specimen that often gets overlooked by visiting researchers in favor of the (often more incomplete) holotype.

What exactly are type specimens for? What is their purpose? According to the ICZN, type specimens are nothing more than a physical record of a species to which a zoological name may be permanently attached. In fact, the use of many historical names through to the modern day demonstrates that holotypes need not even exist - the sperm whale and narwhal do not have type specimens. Extreme cases like this are "grandfathered" in, so to speak, and this practice is no longer acceptable (nor even recommended). Type specimens can even be a plaster cast of a fossil specimen that does not even exist any more, or a single feather plucked from a newly discovered and named but extraordinarily rare "living type" specimen still flying around in the jungles of Borneo. The holotype specimen of the archaeocete Zygorhiza kochii is a relatively useless and miserable shitty braincase without any redeeming features - nobody uses that specimen, and mostly everybody in our field examines USNM 11962, the "de facto reference specimen" which Remington Kellogg monographed in the 1930's.

If the utility of type specimens has no real scientific basis other than mere housekeeping, then there's no real reason we should exclude non-type specimens. I call this weird practice "holotype worship", and I think it moreso has to relate with stamp collecting rather than actual science. Holotype worship - and typological thinking, I believe, are responsible for resistance to many proposed instances of synonymy - the most famous ones that come to mind are the hypotheses that the horned dinosaur Torosaurus is simply an old adult Triceratops, advanced by my close friend John Scannella at Museum of the Rockies, that Nanotyrannus is a juvenile Tyrannosaurus (advanced by Jack Horner and others), and that the dome-headed dinosaurs Dracorex and Stygimoloch are juvenile Pachycephalosaurus, advanced by Mark Goodwin and Jack Horner. Each of these hypotheses incorporates information past holotypes and "de facto reference specimens", uses a larger body of data, and from additional sources - and as a result, arguably explains the fossil record in a superior manner to hypotheses based on fewer data. As an aside, many young folks I've met who are rabidly against John's Torosaurus-Triceratops synonymy hypothesis come from the fanboy part of the spectrum without a strong educational background in science (other than "dinosaurs are cool, ankylosaurus is my favorite"). Other cases of synonymy more relevant to the subject of this blog are the early pinnipedimorphs Pteronarctos goedertae (1989), Pteronarctos piersoni (1990), and Pacificotaria hadromma - which Annalisa Berta argued in 1994 were a single species, a conclusion I tend to follow.

George Gaylord Simpson challenged the focus on holotypes back in 1940, and even then it was apparent that holotype worship was an antiquated form of research from the prior century. Simpson proposed the concept of the Hypodigm - the complete body of all known material assignable to the species under consideration - in other words, the type and all referred specimens. Many researchers have embraced this 75-year old concept, but in some subdisciplines within paleontology there has been surprising resistance. Many older paleontologists are reluctant to let young turks synonymize some of the species they originally named in the process of cementing a long career.  Another pet peeve of mine - and this is particularly relevant to large reviews of various fossil groups - but I've read many papers that flat out only discussed the type species of a particular genus, and ignored those described as additional species within formerly monotypic genera (e.g. a genus with only one species). All fossil species are important! Don't ignore some species just because they were named later (but ignore them if they are synonyms, sure), or worse - don't ignore them because they were named by somebody you don't necessarily like.

Every month I see new papers bringing paleontology into the mid-20th century (and occasionally, late 20th and even 21st centuries) in terms of methods and scope, which gives me hope. Marine mammal paleontology is advancing faster than ever before, largely due to an influx of young researchers attacking new problems with a set of new ideas and tools. Although nearly a century old now, Simpson's idea of the Hypodigm is still as relevant as ever yet hasn't caught on as much as it should. Do your part to help stop "holotype worship" - and use as many specimens as are available!

Berta, A. 1994. New Specimens of the Pinnipediform Pteronarctos from the Miocene of Oregon. Smithsonian Contributions to Paleobiology 78:1-30.

Caretto, P. G. 1970. La balenottera delle sabbie plioceniche di Valmontasca (Vigliano d’Asti). Boll. Soc.
Paleontol. 9: 3–75.

Simpson, G.G. 1940. Types in modern taxonomy. American Journal of Science. 238: 413-431.