Friday, February 28, 2014

Sexual dimorphism in pinnipeds - comments on two new studies in the journal Evolution

Two newly published articles in the journal Evolution investigate the evolution of sexual dimorphism in pinnipeds (seals, sea lions, and walruses). One paper by Kruger et al. (2014) examines it largely from a modern biological perspective, while the other paper by Cullen et al. (2014) incorporates fossil data. We’ll start with Kruger et al., and then move on to Cullen et al.

But first, some introductory remarks. Sexual dimorphism, for the uninitiated, is the condition where males and females of a particular species are of different sizes, color pattern, or proportion (or, all of the above). Naturally this doesn’t apply to anatomical differences in sex organs, as that is something that characterizes practically all vertebrates. Humans are somewhat sexually dimorphic – generally males are taller and more robust than females, and are characterized by some subtle skeletal differences (wider pelves in females, for example). As compared to humans, gorillas are a bit more extremely dimorphic – the males are quite a bit larger, and sport large sagittal crests for jaw muscle attachment on their skulls. Extreme sexual dimorphism has often been linked with reproductive behavior – in particular, “harem” size. In pinnipeds, the males of the least sexually dimorphic species tend to mate with only one female, while males of the most extremely sexually dimorphic species tend to arrange and defend large harems (dozens to hundreds of females) and engage in male-male combat, such as the dramatic fighting commonly seen in elephant seals.

The paper by Kruger et al. (2014) analyzed data on modern pinnipeds including male and female body size, harem size, latitude of breeding, and the length of breeding and lactation, using several phylogenetic comparative methods including phylogenetic independent contrasts and phylogenetic confirmatory path analysis (neither of which I am very familiar with). Their analysis reconstructed ancestral pinnipeds as non-dimorphic and polar in distribution (e.g. Arctic). They further found that sexual dimorphism probably preceded increases in harem size (polgyny); in their words, sexual dimorphism originated first and facilitated polygyny, rather than being a consequence of it. They identify ice breeding as the ancestral reproductive behavior for pinnipeds, rather than aquatic or terrestrial breeding.

Hypothesized sequence of events in the evolution of sexual dimorphism and polygyny in pinnipeds, from Kruger et al. (2014).

There are a few problems with this hypothesis, and most of them revolve around the lack of fossils incorporated into the analysis. Of course, many of the data categories are unknown in fossils (e.g. length of breeding period). However, many fossils indicate that early pinnipeds were in fact sexually dimorphic (Berta 1994; also, see remarks upon Cullen et al., 2014 below). Secondly, simply because many modern pinnipeds breed on ice now doesn’t necessarily mean that they always have, and suggest that this trait is probably unreliable to work with. Tusked walruses, for example, were until only one or two million years ago nearly completely temperate and even subtropical in distribution – only with the evolution of Odobenus rosmarus have walruses been confined to the arctic. Furthermore, Pliocene fossils of Odobenus sp. from Japan indicate that even Odobenus was only cold temperate in distribution roughly 2-3 million years ago. The majority of the walrus fossil record not only reflects sexual dimorphism but also ~20 million years of temperate distribution – in other words, no ice. The early Miocene – the period of pinniped diversification – was substantially warmer than present with smaller icecaps; it makes me wonder if the abundance of modern ice breeding seals is due to recent (Pliocene-Holocene) diversifications into Arctic and Antarctic niches alongside rapidly expanding ice caps. Consider this: the basalmost phocids – monk and elephant seals – are all terrestrial breeding, and several members of the Phoca-Pusa-Halichoerus species complex are terrestrial breeders. It makes much more sense to me that Antarctic lobodontines and Arctic phocines evolved ice breeding habits since the Pliocene during rapid cooling and ice cap growth, rather than all pinnipeds evolving from an ice breeding ancestor and retaining that behavior for 27 million years (in fact, the complex distribution of ice and terrestrial breeding within phocines suggests that if anything, this behavior is really flexible at a macroevolutionary level). A further problem is that the most primitive known fossil pinnipeds, the enaliarctines, are all known from temperate ice-free latitudes. The moral of this story: fossils are important!

New specimen of Enaliarctos emlongi described by Cullen et al. (2014) and interpreted as an adult female.

The new study by Cullen et al. (2014), on the other hand, does incorporate fossil data. They report on a new skull of the early pinniped Enaliarctos emlongi from the Nye Mudstone of coastal Oregon, and performed a geometric morphometric analysis of sexual dimorphism in modern and fossil pinniped skulls. The skull was in fact initially tentatively referred to Enaliarctos emlongi by Annalisa Berta in her 1991 paper on Enaliarctos material from the Emlong collection. The skull is a bit squashed, but appears to be smaller and a bit more gracile than the adult male holotype. Berta (1991) originally considered this specimen to represent a juvenile, although Cullen et al. argue that the sutures are fully closed in the referred specimen, although it’s not immediately obvious from the photographs (a common problem with material in the Emlong collection is that it is consistently dark in color; generally it’s a good idea to coat specimens with ammonium chloride, as has been done by Barnes, Fordyce, Deméré, Berta, and others working on that collection). Sexually dimorphic features they highlight include a narrower rostrum in females, more strongly pronounced nuchal and sagittal crests in males, a proportionally wider palate in males (this probably goes hand in hand with a narrower/broader rostrum in general), and more widely flaring mastoid processes of the squamosal.

Sexually dimorphic features in modern and fossil pinnipeds: Enaliarctos emlongi (left) and Arctocephalus (right); first and third columns are females, second and fourth columns are males.

Morphometric analysis indicated strong sexual dimorphism both in skull size and shape for most pinnipeds, with the exception of numerous extant phocids (true seals - Pusa, Monachus, Erignathus, and Leptonychotes) – of the phocids analyzed, only the gray (Halichoerus) and hooded seals (Cystophora) were strongly dimorphic (Elephant seals, although extraordinarily dimorphic, were not part of the analyzed data set). All otariids, the walrus, and all fossil pinnipeds investigated were dimorphic. When plotted on a cladogram of modern pinnipeds, the ancestral character state is ambiguous owing to widespread lack of dimorphism in the true seals. However, when they incorporated fossil taxa – Enaliarctos and Desmatophoca only – it indicated that sexual dimorphism was primitive for all pinnipeds, and secondarily lost in phocids – and secondarily regained in gray and elephant seals.

Ancestral character state reconstruction of sexual dimorphism in pinnipeds; black=extreme dimorphism, white=little to no dimorphism. Top tree includes extant pinnipeds only, and bottom tree shows the influence of the inclusion of fossil taxa.
Overall, this publication by Cullen et al. is vastly superior in its treatment of sexual dimorphism in pinnipeds, particularly for its inclusion of fossils – which is unsurprising, since the authors are all paleontologists. I strongly suspect that Cullen et al. are correct, and this paper serves to reinforce earlier suggestions that enaliarctines were sexually dimorphic. However, there are a few minor nitpicky things that bear mentioning.

First, it is important to note that this study is not the first to propose that enaliarctines were sexually dimorphic. In fact, the first study to demonstrate sexual dimorphism was the reevaluation of Pteronarctos by Annalisa Berta (1994) – in that paper, she examined a large collection of material from the Emlong collection and concluded that Pteronarctos piersoni and Pacificotaria hadromma were prematurely named, and fall within the range of variation expected for a single species of pinniped (based on examination of variation in extant Callorhinus ursinus), and synonymized both species with Pteronarctos goedertae (regardless, later works by Barnes have been uncharitably dismissive of this hypothesis). Berta (1994) ascribed much of the variation between species to sexual dimorphism, and identified the holotypes of P. piersoni and P. hadromma as females (also dismissed by recent work by Barnes), in addition to figuring and describing additional female specimens of Pteronarctos goedertae from the Emlong collection. Curiously, this acknowledgement of sexual dimorphism in Pteronarctos was not mentioned or cited by Cullen et al. (2014), despite citing the paper. Sexual dimorphism in enaliarctines has also been suggested in various papers by Larry Barnes (1989, 1990, 1992, 2008), and demonstrated in the enaliarctine-like proto-walrus Proneotherium repenningi (Deméré and Berta 2001).

Secondly, the entire crux of this paper hinges upon the identification of the referred skull, USNM 314290 as being conspecific with Enaliarctos emlongi. I’ve never seen the specimen (it was on loan in Canada when I visited the USNM to examine their pinnipeds in 2012), but a few things struck me with the description. For starters, it was only compared with Enaliarctos emlongi, Enaliarctos barnesi, and Enaliarctos tedfordi. What about Pteronarctos? Pteronarctos is, after all, known from really low down in the Astoria Formation – around the same level as some Enaliarctos material reported by Berta (1991). No comparisons with Pinnarctidion are made, and most problematic, no comparisons with Enaliarctos mitchelli are made – Enaliarctos mitchelli is tiny, with a transversely narrow rostrum (consistent with USNM 314290) and known from the Nye Mudstone of Oregon (Berta 1991) in addition to Pyramid Hill in California. I could easily see this specimen representing another E. mitchelli specimen – but that possibility was not evaluated.

This study by Cullen et al. (2014) is certainly an excellent contribution, and a great starting point. Future analyses can (and, should) utilize other fossil pinnipeds for which males and females are known: Allodesmus gracilis/kernensis, Dusignathus seftoni, Imagotaria downsi, Neotherium mirum, Proneotherium repenningi, Pteronarctos “spp.”, Thalassoleon mexicanus, and Valenictus chulavistensis (some of these are known from male and female mandibles only (e.g. Neotherium). And of course, there’s also canines, postcrania, and that curious baculum.

A parting comment is necessary, and this should not be misconstrued as further criticism, but a word of caution for any study regarding the phylogenetic position of fossil pinnipeds: We currently do not have a robust up-to-date phylogeny for modern and fossil pinnipeds. It’s now been twenty years since Berta and Wyss (1994) published their seminal analysis of modern and fossil pinniped phylogeny, and nobody has taken up the challenge of adding more characters and taxa to that dataset (or, even putting together a new dataset of equivalent breadth). Most subsequent studies have incorporated taxa only from a single family (and this is something I am definitely guilty of). Although not stated by the authors, the phylogenetic position of Enaliarctos and Desmatophoca are probably from Berta and Wyss (1994). Morgan Churchill and I have talked about these issues at length, and we wouldn’t be surprised if 1) desmatophocids were more closely related to otarioids than phocids, 2) morphological evidence could be mustered to support an odobenid-otariid clade, and 3) enaliarctines might actually be more closely related to otarioids than to phocoids. What can be done about this? Cullen et al. (2014) rightfully point out that enaliarctines are greatly in need of a taxonomic enema (my paraphrasing): they are probably greatly oversplit, and a detailed comprehensive study of enaliarctine morphology is in order – this is especially true if Berta’s (1991) lumping of Pteronarctos goedertae, Pteronarctos piersoni, and Pacificotaria is any indication. In addition to a better treatment of enaliarctines, we need a larger analysis of pinniped phylogeny, with more taxa. Morgan and I started a such a project several years ago and presented it at SVP, and then decided it would be best to treat each family one at a time before doing anything comprehensive – but, more on that in the future.

References and further reading:

L. G. Barnes. 1989. A new enaliarctine pinniped from the Astoria Formation, Oregon, and a classification of the Otariidae (Mammalia: Carnivora). Contributions in Science 403:1-26

L. G. Barnes. 1990. A new Miocene enaliarctine pinniped of the genus Pteronarctos (Mammalia: Otariidae) from the Astoria Formation, Oregon. Contributions in Science 422:1-20

L. G. Barnes. 1992. A new genus and species of middle Miocene enaliarctine pinniped (Mammalia, Carnivora, Otariidae) from the Astoria Formation in Coastal Oregon. Contributions in Science 431:1-27

L. G. Barnes. 2008. Otarioidea. In C. M. Janis, G. F. Gunnell, M. D. Uhen (eds.), Evolution of Tertiary Mammals of North America 2:523-541

A. Berta. 1991. New Enaliarctos* (Pinnipedimorpha) from the Oligocene and Miocene of Oregon and the role of "enaliarctids" in pinniped phylogeny. Smithsonian Contributions to Paleobiology 69:1-33

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

A. Berta and A. R. Wyss. 1994. Pinniped phylogeny; pp. 33–56 in A. Berta and T. A. Deméré (eds.), Contributions in Marine Mammal Paleontology Honoring Frank C. Whitmore, Jr. Proceedings of the San Diego Society of Natural History 29.

T.M. Cullen, D. Fraser, N. Rybczynski, and C. Schroder-Adams. 2014. Early evolution of sexual dimorphism and polygyny in Pinnipedia. Evolution DOI: 10.1111/evo.12360

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

N. Kohno, 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

O. Kruger, J.B. Wolf, R.M. Jonker, J.I. Hoffman, and F. Trillmich. 2014. Disentangling the contribution of sexual selection and ecology to the evolution of size dimorphism in pinnipeds. Evolution DOI: 10.1111/evo.12370

Tuesday, February 25, 2014

The Eocene - rather than Oligocene - origin of modern whales (Neoceti)

Back in early 2014 I wrote this post with a much more limited body of available literature - there were several things I knew about at the time but could not discuss. So, six years later, after the publication of Llanocetus, Mystacodon, Olympicetus, Fucaia, and others, it's time to revisit and update this post.

Baleen whales (Mysticeti) and toothed whales (Odontoceti) are nearly universally considered to share a sister-group relationship, and constitute a monophyletic clade termed Neoceti (also known as Autoceta). Odontocetes and mysticetes are generally considered (until recently) to have diverged and diversified during the Oligocene, and neither group really has an extensive fossil record prior to the Oligocene. On the other hand, archaeocetes – a paraphyletic assemblage of stem cetaceans leading up to neocetes – generally are considered to be restricted to the Eocene (though conference abstracts from my doctoral lab by Josh Corrie and my adviser Ewan Fordyce suggest that kekenodontids are late surviving Oligocene archaeocetes). For paleocetologists, the Eo-Oligocene boundary is colloquially thought of as the archaeocete-neocete split. However, many early Oligocene neocetes are relatively derived, and few are really archaeocete-like – in other words, few appear to exhibit archaeocete-like morphology with only a couple of acquired neocete synapomorphies. This begs the question of when exactly Neoceti evolved.


 The holotype skull of the early Oligocene dolphin Simocetus rayi - from the Alsea Formation of Oregon. I photographed the original specimen in spring 2016 at the Smithsonian.

Early Oligocene Neoceti: Alsea Formation, Oregon

The majority of the Oligocene record of fossil cetaceans is limited to the late Oligocene (owing to generally low sea levels and widespread erosion of early Oligocene strata), but a few notable records of early Oligocene cetaceans are worth discussing. In particular are the fossil cetaceans of the Alsea Formation in west central Oregon. Although considered by Fordyce (2002) to be late Oligocene, paleomagnetic data indicate it is probably early Oligocene in age (Prothero, 2001). First and foremost is Simocetus rayi – the only formally described cetacean from this unit, a bizarre agorophiid-grade dolphin described by Fordyce (2002). Simocetus is pretty derived, and not really archaeocete-like in many regards. Another agorophiid-grade dolphin is an unnamed tusked odontocete, preliminarily reported by Fordyce et al. (2012) at the Society of Vertebrate Paleontology meeting in Raleigh, North Carolina. This undescribed dolphin is also fairly derived and fairly removed from the odontocete stem. (Reidentified by Peredo et al. 2019 as a xenorophid, which I don't necessarily buy - given that xenorophids are highly autapomorphic and restricted to Oligocene strata in the Carolinas). A third cetacean from the Alsea Formation is the world’s earliest toothless mysticete (an eomysticetid in my personal opinion), recently named Maiabalaena nesbittae by Peredo et al. (2018). A fourth cetacean which I spotted at the USNM in 2012 is an undescribed aetiocetid with a complete braincase and somewhat basilosaurid-like mandible. Yet another aetiocetid is known, but is currently under study by C-H Tsai and myself, and I won’t spoil it. The Alsea Formation demonstrates that the early Oligocene was populated by the same sorts of cetaceans known from the late Oligocene. Most notably, the presence of an early chaeomysticete (Maiabalaena) – in my opinion an eomysticetid – indicates that mysticete evolution is telescoped into a 5 million year interval (or less), given our current understanding of the timing of mysticete origins. 


 The two species of Fucaia from the Oligocene of Washington - not to scale! On the left is Fucaia buelli (UWBM collections) from the early Oligocene (Makah Formation), and on the right is Fucaia goedertorum (LACM collections), from the "middle" to late Oligocene Pysht Formation. Both specimens were discovered and collected by the Goederts.

The two original skulls of Olympicetus avitus published by Jorge Velez-Juarbe. Olympicetus is not really discussed in this post, but there are undescribed Simocetus/Olympicetus like dolphins from the older Makah Formation. Image by Jorge Velez-Juarbe.

Life reconstruction of a juvenile cf. Olympicetus specimen we published - and which we hypothesized was unable to echolocate - and therefore reconstructed here without a melon, and a bit of an archaeocete like face (albeit much, much cuter!). Artwork by me!

 A partial skill with associated mandible, vertebrae, and bulla of a Simocetus-like dolphin from the Makah Formation - from CCNHM collections. Collected, and generously donated to us, by Jim Goedert. This was my first serious acid preparation project - this is after a couple months of acid prep. It's been fully prepped out for a couple years and I'm working on describing it - it's one of the most plesiomorphic odontocetes in existence and has some very... interesting teeth.

Early Oligocene Neoceti: Makah Formation, Washington

 The lower Oligocene Makah Formation is one of three Oligo-Miocene units on the strait of Juan de Fuca on the north coast of the Olympic Peninsula of Washington; it is overlain by the “middle” to upper Oligocene Pysht Formation and in turn by the lower Miocene Clallam Formation. The Makah is about the same age as the Alsea, but with a slightly older base at about 33.2 - 31 Ma. The first formally described cetacean from the Makah Formation is the tiny toothed mysticete Fucaia buelli named by Felix Marx et al. in 2015. It is quite similar to Chonecetus goedertorum from the overlying Pysht Formation, which the authors reassigned to Fucaia. These toothed mysticetes still had shearing wear facets on their teeth, and may not have had baleen (as proposed for other aetiocetids like Aetiocetus and Morawanacetus; though I will cover this later).


One of the most plesiomorphic (primitive) looking baleen whales ever discovered - Coronodon havenstein, from the lower Oligocene Ashley Formation. It's basically 75% archaeocete in terms of its skull shape, but we think it was able to filter feed with its teeth (no proto-baleen). On display at CCNHM. Mystacodon is slightly more primitive in its morphology but usually plots out a node further crownward (as a sister taxon to Llanocetus).

Also from the Ashley Formation - straight from the title of the paper - "an unexpectedly derived odontocete" - Ediscetus osbornei. This is a Waipatia-like or waipatiid-grade dolphin from the Ashley - at least a couple million years older than the oldest waipatiids from NZ, but possibly somewhat more derived owing to a more telescoped vertex. From Albright et al., 2018.

Early Oligocene Neoceti: Ashley Formation, South Carolina

 The Ashley Formation is somewhat younger than the Alsea or Makah formations, but is known from a substantially more diverse cetacean fauna of late early Oligocene age (e.g. late Rupelian - ~30-28 Ma). Mysticetes include Coronodon havensteini, the eomysticetid Micromysticetus rothauseni, and at least one strange chaeomysticete I collected a couple years ago that may be related to the fragmentary but strange New Zealand mysticetes Toipahautea and Whakakai. Odontocetes include Agorophius pygmaeus, a handful of xenorophids (Xenorophus sloanii, Albertocetus meffordorum, Inermorostrum xenops), the recently re-named Ankylorhiza tiedemani, and one of the most archaic known dolphins ever discovered – Ashleycetus planicapitis. Several additional odontocetes, including the simocetid-like rostrum referred to Agorophius pygmaeus by Fordyce (1981), and a dwarf Agorophius, are also known and await description by yours truly. Most recently, and most surprisingly, is a Waipatia-like dolphin, Ediscetus osbornei – possibly belonging to the Waipatiidae, but there have been some problems with diagnosing and defining this clade. Waipatia and Ankylorhiza are the most derived odontocetes from the Ashley Formation – yet again, pushing even more nodes and divergences further back into the early Oligocene. Perhaps what is most shocking about the Ashley Formation is its diversity: there are over a dozen species of cetaceans present. In contrast, the most diverse Eocene cetacean assemblages have half that (~5-6) - and most have only a quarter of that diversity (~3 species, like the Jackson Group on the Gulf coastal plain of the USA).


Early Oligocene Neoceti: Ototara & Amuri imestones, New Zealand

 An interesting skull, the "protosqualodont of Keyes", was collected from a famous limestone quarry near Oamaru (Parkside Quarry*) on the South Island of New Zealand. I never ended up going to that quarry, since the limestone is shockingly vertebrate poor - and I cannot recall if discovered from the quarry or an exposure elsewhere of the Ototara Limestone, but the gigantic thick-boned penguin Pachydyptes ponderosus was also discovered in this unit.


The "protosqualodont" of Keyes is a likely llanocetid, and one of the oldest known Neoceti from New Zealand. I cannot for the life of me find the published image of the skull in a block, so here are a couple of the preserved teeth of OU GS 10897 from Keyes (1973).

The "protosqualodont" was originally reported by Ian Keyes (1973), who was best known for publishing an excellent series of articles on fossil sharks from New Zealand. The teeth were quite strange - at the time, a number of poorly known isolated cheek teeth of highly variable shapes had been reported from the Oligocene and lower Miocene of Australia and New Zealand, with many named as different species of Squalodon, Parasqualodon, and Metasqualodon - all tooth-based taxa. Mention these in front of Ewan and he'll furrow his brow and say something like "quite difficult taxa, pity". Indeed, most of these are isolated teeth and difficult to diagnose or even assess in terms of diversity. These assemblages were all we had for decades in Australia and New Zealand - and now appear to represent odontocetes, toothed mysticetes, and kekenodontids (I will not be specific, owing to unpublished research). The "protosqualodont" was different, though, because it was a set of associated teeth. At the time, Keyes (1973) considered these the oldest cetacean remains from New Zealand - indeed, the Ototara Limestone dates to 33-32 Ma, which is approximately earliest Oligocene. Originally discovered in the matrix associated with a bone fragment - and misidentified as a partial mandible by Keyes owing to its flatness, and later reidentified in Fordyce's (1979) Ph.D. thesis as the top of the skull. The presumed molar is quite low crowned, with very rugose enamel, and a vestigial third root; the top of the braincase is generally similar to mammalodontids in its flatness. Later, Ewan visited a private collector who happened to have a partial cetacean skull in a block of limesstone from the same quarry - which happened to be the rest of the skull! This specimen, OU GS 10897 - now appears to be a small bodied llanocetid-like toothed mysticete.

 *Parkside Quarry is a source of bryozoan limestone facies of the Ototara Limestone - known commercially locally as "Oamaru stone", which is sought after for its desirable characteristics for stone carving. Many Māori artists use the stone to carve koru (a spiral shape after unfurling tree fern fronds, a symbol of new life/growth), wheku (stylized carving of a face), and Muri paraoa (a whale tail; I received a greenstone carving of one from Ewan on my day in NZ, a tradition for advisers to give to their students, and I have it hanging on my PhD diploma in my office). I always wanted a Muri paraoa carving for obvious reasons, but we could never afford one.


ZMT 67, a partial toothed mysticete mandible from the Amuri Limestone, South Island, New Zealand. This specimen is one of the oldest Neoceti from Australasia and is a possible llanocetid according to some of our analyses in Geisler et al. (2017) - photos from a book chapter by R.E. Fordyce.

Another specimen from New Zealand is a mandible fragment from the earliest Oligocene Amuri Limestone, which Fordyce (1989) identified as a possible toothed mysticete. The specimen preserves some partial teeth, which had numerous cusps in a radial pattern (a mysticete synapomorphy we proposed in our 2017 paper on Coronodon), double rooted molars, and embrasure pits – the mandible is also very shallow, unlike the tall, narrow mandible of Llanocetus. We actually coded the highly fragmentary specimen into our cladistic analysis for Coronodon, and it came out between Coronodon and aetiocetids (like Fucaia) - far removed from Llanocetus. However, our codings for Llanocetus were based on what was available from the literature before the skull was published upon - codings of the available mandible, and skull codings from Fitzgerald (2010). So, this position has changed. I personally think that ZMT 62 is probably a small bodied llanocetid.

In summary - while not as common as fossil assemblages dating to the late Oligocene, early Oligocene cetacean assemblages include at least a few species of mysticetes, an eomysticetid, and a few species of odontocetes. There are a few interesting things to consider: 1) early Oligocene faunas, despite being depauperate relative to late Oligocene faunas, still show some inkling of diversity - the late early Oligocene Ashley Formation being the most extreme (~10-15 cetaceans). 2) Many of these early Oligocene cetaceans are quite derived - examples include aetiocetids (Fucaia), eomysticetids (Maiabalaena, Micromysticetus), agorophiid-grade dolphins (Ankylorhiza), and waipatiid grade dolphins (Ediscetus). These taxa co-occur with more plesiomorphic cetaceans (e.g. Simocetus, Coronodon, Xenorophidae) and imply some ghost lineages at least a few million years long. 3) Another major contrast is body size - most of these, with the exception of Llanocetus, Coronodon, eomysticetids, and Ankylorhzia, are small. Most Oligocene odontocetes are smaller than a modern bottlenose dolphin; most toothed mysticetes, the mammalodontids and aetiocetids in particular, are downright tiny: harbor porpoise sized at the smallest (Fucaia buelli) and only a few that exceed a bottlenose dolphin in size (Aetiocetus), approaching the size of a pilot whale. We're still working this one out, but in concert with an explosive diversification in feeding morphology, it's likely related to changes in feeding and ecology across the Eocene-Oligocene boundary. 4) There is evidence of regional differences in faunas as early as the early Oligocene: simocetids and aetiocetids dominate North Pacific cetacean assemblages; xenorophids, agorophiid-grade dolphins, and Coronodon are only in North Atlantic assemblages; and New Zealand and Australia preserve mammalodontids, llanocetids, kekenodontids, and waipatiids (the latter shared with the North Atlantic). Only the Eomysticetidae are found in every basin during the Oligocene (now found in Oligocene rocks from Australia, New Zealand, Japan, Washington, Baja California (Mexico), North and South Carolina, and Austria. All of this evidence from the early Oligocene is highly suggestive of a many ghost lineages that should be illuminated by further collecting from earlier strata.


Holotype mandible fragment of the late Eocene mysticete Llanocetus denticrenatus from the La Meseta Formation of Seymour Island. From Mitchell (1989).


The large, and bizarre, skull of Llanocetus denticrenatus; latest Eocene, La Meseta Formation, Seymour Island, Antarctica. From Fordyce and Marx (2018).

Known records of neocetes in the Eocene

 As could be surmised from the presence of relatively derived Neoceti in the early Oligocene, a few – but only a few – records of latest Eocene mysticetes and odontocetes exist. First and foremost, the only named Eocene neocete is the earliest known baleen whale, Llanocetus denticrenatus from the La Meseta Formation of Seymour Island in Antarctica. It was named by Ed Mitchell in 1989, and the miserable scraps he designated as the holotype were originally collected in the mid 1970’s. My Ph.D. adviser, Ewan Fordyce, returned to the locality in 1986 and collected the rest of the specimen, which is a rather large skull and mandible in addition to some postcrania. The bizarre skull, complete with a markedly flattened rostrum, teeth with some basilosaurid-like features and very wide diastmata (gaps between teeth), was recently published by Fordyce and Marx (2018). The type specimen dates from just below the Eo-Oligocene boundary and is approximately ~34 Ma in age. Accordingly, Llanocetus is quite archaic - though nowhere near as basilosaurid-like as Coronodon havensteini, which we named in 2017 (Geisler et al.); accordingly, Llanocetus typically plots out a node or so crownward of Coronodon, despite being older - suggesting that the lineage split even earlier during the Eocene.


An apparent second, and larger (but as yet, unnamed) species of Llanocetus exists - discovered recently and known mostly from isolated teeth. Interestingly, the new tooth bears a somewhat closer shape to that of the "protosqualodont" of Keyes (1973). The premolar of Llanocetus denticrenatus is on the left, and the premolar of the unnamed larger taxon, Llanocetus sp., is on the upper left.

In early 2017, the world was introduced to Mystacodon selenensis – a medium sized toothed mysticete with a narrow rostrum from the uppermost Eocene Yumaque Formation of Peru. Mystacodon has basilosaurid-like flippers, but with a locked elbow joint – a clear neocete feature. The teeth are highly heterodont and similar to a basilosaurid. The skull is decidedly basilosaurid-like but has a slightly more telescoped vertex with a triangular occipital shield, and more posteriorly placed nares - surprisingly similar to a skull of a NZ kekenodontid (OU 22294) figured by Clementz et al. (2012). Subsequent studies have supported a close relationship with Llanocetus, with Fordyce and Marx (2018) assigning it to the Llanocetidae along with the “protosqualodont”.


The skull, teeth, and beautifully preserved pelvis of the basilosaurid-like toothed mysticete Mystacodon selenensis from the uppermost Eocene Yumaque Formation of Peru. From Muizon et al., 2017.

There is also an undescribed odontocete preliminarily reported from about the Eo-Oligocene boundary within the Lincoln Creek Formation in Washington state, U.S.A. (Barnes and Goedert, 2000). Another specimen, collected by Jim Goedert, is a putative chaeomysticete from the late Eocene part of the Lincoln Creek Formation – if the dating is accurate.* These specimens – although only barely scraping into the Eocene – do demonstrate that odontocetes and mysticetes did evolve before the end of the Eocene.

 *Ironically, I first learned of this specimen when I first wrote this post six years ago; I received an email out of the blue from Jim Goedert. I then saw the specimen in person at the Burke Museum in January 2016 – it’s definitely an eomysticetid-like chaeomysticete, and has toothless mandibles and a poorly telescoped braincase. This specimen is highly fragmented and needs lots of careful preparation, and is begging for study. If accurately dated, it would upend even much of the divergence dates pushed back by the discoveries outlined here in this blog post. See “Caveats” for more.


 The calibrated phylogenetic tree of Cetacea with molecular divergence dates (horizontal gray bars) - showing the basamost nodes of Neoceti diverging in the Eocene. A middle-of-the-road result, albeit based on the time on fossils that had not been published. From McGowen et al. (2009).

What does Molecular divergence dating tell us?

 Molecular clock dating is a popular – if sometimes limited – method of estimating divergences between clades. Unfortunately, we’re obviously limited to branches between extant species – and in many cases, morphological phylogenies do not recover the same relationships between extant species – calling into question over which has it right. Another issue is that the rate can be very different from what we see in the fossil record – with molecular divergence dates sometimes pre-dating paleontological evidence by tens of millions of years (the origin of modern placental mammals relative to the Cretaceous-Paleogene extinction is a classic example). Unless properly calibrated with carefully selected fossils with a clearly known phylogenetic position, divergence dates can be off quite a bit.

 Many studies have inferred an Eocene divergence of Neoceti – and in some cases, owing to the use of Llanocetus as a calibration point (e.g. McGowen et al., 2009). Perhaps the most prominent cladistic analysis of cetaceans published in recent years, Geisler et al. (2011) eliminated unpublished fossils from their list of fossil calibrations – and in so were forced to ignore Llanocetus, which at the time was only known by the original fragments published by Mitchell (1989). The late Eocene age was clearly known – but relationships as a toothed mysticete could not be resolved based upon the scrappy mandibular fragment. As a result, the divergence of Neoceti was dated to the early Oligocene. A recent analysis went so far as to date the divergence of crown Odontoceti as occurring during the late middle Eocene – despite no crown odontocetes being demonstrably known from the late Oligocene or earlier (McGowen et al., 2020). In contrast, the more conservative analysis of Geisler et al. (2011) recovers the divergence of Crown Odontoceti in the early Oligocene. This is still interesting to me, as the earliest diverging extant odontocetes – the sperm whales – have a strictly post-Oligocene fossil record, with the possible exception of the fragmentary Ferecetotherium, known mostly from teeth and a mandible from the latest Oligocene of Azerbaijan.

There are a *ton* of different studies I have glossed over, and there's likely something I've missed. Regardless, at this point there is clear support from molecular clock analyses for an Eocene origin of odontocetes. But how early?


The earliest Basilosauridae – middle Eocene

One problem inherent with a late or even latest Eocene origin of Neoceti is that it would telescope the majority of basilosaurid evolution into a 5 Ma period during the Priabonian and late Bartonian stages of the Eocene. The oldest records of traditionally identified basilosaurids are only about 40 Ma, only 5-6 Ma older than Llanocetus. However, a recent discovery of a basilosaurid from the Bartonian (late Middle Eocene) of Ukraine suggests a reinterpretation of “Eocetuswardii from similarly aged strata in the eastern USA. Gol’din and Zvonok (2013) named a new genus and species, Basilotritus uheni – which has vertebrae like “Eocetuswardii with the tympanic bulla of a basilosaurid. Gol’Din and Zvonok (2013) transferred “Eocetuswardii to Basilotritus, recombining it as Basilotritus wardii. In addition to the recognition of both species of Basilotritus as early basilosaurids, a couple other middle Eocene basilosaurids have been reported, including a braincase from the Bartonian of New Zealand identified as Zygorhiza sp. (Kohler and Fordyce, 1997), and Ocucajea and Supaycetus from the Bartonian of Peru (Uhen et al., 2011). Unfortunately, the protocetid-basilosaurid transition is poorly known, although several protocetids exhibit derived basilosaurid-like features, including Georgiacetus, Babiacetus, and Eocetus, and the earlier basilosaurids like Basilotritus and Supaycetus are a bit more plesiomorphic than other basilosaurids. 


Phylogenetic relationships and stratigraphic ranges of Basilosauridae, from Gol'Din and Zvonok (2013).

Along with an earlier divergence of Neoceti, and the extremely primitive anatomy of early toothed mysticetes like Coronodon and Mystacodon, the possibility is raised – how different would the earliest neocetes actually look from basilosaurids? Are basilosaurids actually before the split? The limited descriptions available for some, and limited cranial material for most, could allow for this sort of situation. Godfrey et al. (2012) go so far as to highlight that, in a description of a partial skull of unknown age, that the earliest mysticetes and odontocetes could even grossly resemble protocetids in their skull anatomy. This again is the same problem highlighted above regarding molecular versus morphological divergence: anatomical features may change much more slowly and manifest after the molecular split, in which case we would have no way of knowing (save for broader taxon sampling and extremely careful coding) if some basilosaurids were in actuality stem odontocetes or stem mysticetes. Personally, all archaeocete groups are admittedly paraphyletic anyway, and I see this as probable but likely (at this point) intractable.


Why are there no late Eocene Neoceti from Egypt or the southeastern USA? Some thoughts, and caveats

This is the question that really chaps my ass. Where are the dolphins and mysticetes from the Jackson Group of the gulf coast - latest Eocene - very well-sampled strata - or, from the most meticulously sampled (and beautifully exposed) whale-bearing late Eocene rocks anywhere in the world: Egypt?

The short answer is, I have no clue. Long, rambling answer: It’s worth noting that late middle and early late Eocene assemblages from South Carolina and Morocco have some similarities (pappocetine protocetids, Chrysocetus), and there are genus-level similarities with the late Eocene of the southeast USA and Egypt in general (Basilosaurus, Dorudon, ?Cynthiacetus). It’s not perfect – not like the similarities between Pliocene marine mammals from Europe and the eastern USA – and perhaps archaeocetes were less pelagic than modern cetaceans (hardly an unreasonable hypothesis), therefore having more regional provincialism. With only a little data, it’s tempting to suggest that perhaps the North Atlantic and Tethys were a single biogeographic province, dominated by archaeocetes. 


A specimen of
Saghacetus osiris, a typical basilosaurid from the latest Eocene of Egypt. It's not radically different from Zygorhiza, Basilosaurus, or Cynthiacetus from the Gulf Coastal Plain of the southeastern USA - though only 2-3 million years older than the oldest odontocetes, and contemporaneous with the oldest mysticetes in the south Pacific. Image from Ghedoghedo on Wikipedia.

What’s the point of all this? All examples of Eocene Neoceti are either from the eastern Pacific or from the Antarctic peninsula, on the fringes of the Pacific: Lincoln Creek Formation of Washington, USA; Yumaque Formation, Peru; La Meseta Formation, Seymour Island, Antarctica). Some bona fide archaeocetes are known from late Eocene assemblages from the Pacific (Zygorhiza sp., New Zealand; Cynthiacetus peruvianus, Peru), but these assemblages are not exclusively dominated by archaeocetes like known assemblages in the Atlantic-Tethyan province is. So, maybe there is a regional difference. In which case – more Eocene rocks along the Pacific margin clearly need to be explored. There are some Eocene marine deposits in California and Oregon [stay tuned…] which are sure to eventually produce some cetacean remains. I’m also convinced that more Eocene-Oligocene deposits probably exist further north in the Pacific Northwest, in British Columbia and southern Alaska. There are tons of Oligocene cetaceans from Japan, and no shortage of Eocene mollusks. I have a hard time believing there were no cetaceans there during the Eocene. I also wonder about the Korean peninsula and coast of China. On the other hand, where there’s smoke, there’s fire: sometimes it’s easier to attack a known fossil site then to discover new ones. In which case, further field investigation of the Lincoln Creek Formation (and the Yumaque Formation of Peru) seems like an obvious choice.

Lastly, caveats. One issue that comes up time and again is that most of the ages for deposits in the Pacific northwest stem from a single edited volume (Prothero, 2001) and I’ve heard many private grumblings about the quality of the paleomagnetic analyses published within (politely refraining from repeating them here), and read some published responses (Nesbitt et al., 2010). So, it’s possible that these paleomagnetic analyses could be off by one or more reversed or normal chrons – paleomagnetism is out of necessity done in concert with biostratigraphy, typically foraminifera or perhaps diatoms. In the Pacific Northwest, most of the micropaleontological work has been done with benthic foraminifera rather than planktonic foraminifera – the latter is much, much more accurate than the former, and so the biochronology of mid Cenozoic Pacific Northwest stratigraphy is, for the time being, a bit hamstrung. So many of these surprisingly derived simocetids and eomysticetids from the earliest Oligocene may be a bit younger. That being said, this has no bearing on cetaceans of similar evolutionary stage showing up in the 28-30 Ma Ashley Formation, dated to late Rupelian with forams, strontium, and – if I recall correctly – dinoflagellates as well. So, there would have to be *pervasive* mis-dating of early Oligocene cetacean assemblages worldwide in order for dating to be a viable problem.



In summary, there are several derived neocetes (Ediscetus, Ankylorhiza, Maiabalaena, Micromysticetus) from the early Oligocene, and in some cases forming diverse assemblages, a couple of genuine records of Neoceti from the latest Eocene (Mystacodon, Llanocetus) – and lastly, the expanded fossil record of basilosaurids now ameliorates the problem of a formerly telescoped record of the family. More records of early odontocetes and mysticetes from the Eocene does not sound like such a strange idea anymore, but is in fact now predicted by the fossil record. We have little evidence of it, but improved sampling of late Eocene marine rocks – especially from poorly sampled areas (in terms of Eocene rocks) like the Pacific Northwest, the west coast of South America, and possibly Japan, the Korean peninsula, and China – may yield more records of early Neoceti.


 References Cited

Albright et al. 2018.

L. G. Barnes and J. L. Goedert. 2000. The world's oldest known odontocete (Mammalia, Cetacea). Journal of Vertebrate Paleontology 20(3):28A.

Fordyce, 1989.

R. E. Fordyce. 2002. Simocetus rayi (Odontoceti, Simocetidae, new family); a bizarre new archaic Oligocene dolphin from the eastern North Pacific. Smithsonian Contributions to Paleobiology 93:185-222.

Fordyce and Marx, 2018.

R.E. Fordyce, E.M.G. Fitzgerald, G. Gonzalez Barba. 2012. Long-tusked archaic odontocetes from Oregon and Baja California Sur, eastern Pacific Margin. Journal of Vertebrate Paleontology 32:3:95.

Geisler et al., 2011.

Geisler et al., 2017.

Godfrey et al., 2012.

P. Gol'din and E. Zvonok. 2013. Basilotritus uheni, a New Cetacean (Cetacea, Basilosauridae) from the Late Middle Eocene of Eastern Europe. Journal of Paleontology 87(2):254-268.

Keyes, 1973.

R. Kohler and R. E. Fordyce. 1997. An archaeocete whale (Cetacea: Archaeoceti) from the Eocene Waihao Greensand, New Zealand. Journal of Vertebrate Paleontology 17(3):574-583.

Lambert et al., 2017.

Marx et al., 2015.

Marx et al., 2019.

McGowen et al., 2009.

McGowen et al., 2020.

E. D. Mitchell. 1989. A new cetacean from the late Eocene La Meseta Formation, Seymour Island, Antarctic Peninsula. Canadian Journal of Fisheries and Aquatic Sciences 46(12):2219-2235.

Muizon et al., 2018.

Nesbitt et al., 2010.

Peredo et al., 2018.

Peredo et al., 2019.

Prothero DR, Bitboul CZ, Moore GW, Niem AR. 2001. Magnetic stratigraphy and tectonic rotation of the Oligocene Alsea, Yaquina, and Nye formations, Lincoln County, Oregon. In: Prothero DR, ed. Magnetic stratigraphy of the Pacific coast Cenozoic. Pacific Section SEPM (Society for Sedimentary Geology) 91:184–194.

M. D. Uhen (2007): The earliest toothless mysticete: A chaeomysticetan from the early Oligocene Alsea Formation, Toledo, Oregon. – Journal of Vertebrate Paleontology 27/3 Suppl.: 161A.

M. D. Uhen, N. D. Pyenson, T. J. DeVries, M. Urbina, and P. R. Renne. 2011. New middle Eocene whales from the Pisco Basin of Peru. Journal of Paleontology 85(5):955-969.

Thursday, February 6, 2014

Coastal Paleontology in the News: recent press coverage, new publication in Geodiversitas

It's been about four weeks since I posted something on here last, but I've got some new stuff coming up. To kick it off, I have finally gotten around to submitting a press release about my new publication in Geodiversitas (in all actuality, published on December 27 of last year). What took me so long? I needed a suitable image for the press release, so I waited until I had completed a new piece of artwork. More on that below.

The new paper in Geodiversitas is concerned with a fossil assemblage of marine mammals from a relatively young section of the Purisima Formation. Most marine mammal fossils from the Purisima Formation are a bit younger, being from the latest Miocene; few well-preserved specimens are known from the Pliocene sections. Plenty of other latest Miocene marine mammal assemblages in California and Baja California exist, including the Capistrano and San Mateo Formations of Orange and San Diego Counties, and the Almejas Formation of Cedros Island off the Baja California Peninsula. However, pretty much only one Pliocene marine mammal assemblage exists for comparison - the San Diego Formation.

With this in mind, I began digging up marine mammal fossils over two two-year periods, each covered by a paleontological collections permit from California Parks and Rec. It took years to complete preparation, curation, and study the hundreds of fossils uncovered during this study, but ultimately this project produced three separate publications. The first covered the sharks, bony fish, and marine birds, while the second reported on the youngest fossil of a bony toothed bird from the Pacific basin. Although titled "A new marine vertebrate assemblage from the Late Neogene Purisima Formation in Central California, part II: Pinnipeds and Cetaceans", technically speaking the pelagornithid article was really the second part, but my coauthor Adam Smith wasn't too keen having such a long title.

One fossil in particular, the skull that would eventually become the holotype specimen of Balaenoptera bertae named in this paper, was collected when I was 19 years old. It was my first real excavation, and the first time I had ever made a plaster jacket. I'll have a longer post about the collection of the holotype later on down the line.

The fossil assemblage eventually yielded 21 marine mammals, for a total of 34 marine vertebrates. The assemblage includes fur seals (Callorhinus), walruses (Dusignathus), a "river" dolphin (Parapontoporia sternbergi) related to the recently extinct (ca. 2007) Baiji, several porpoises (Phocoenidae, unnamed genus 1, unnamed genus 2, cf. Phocoena sp.), a delphinid dolphin, a globicephaline pilot whale, two species of dwarf baleen whales (Herpetocetus bramblei, Herpetocetus sp.), the archaic balaenopterid "Balaenoptera" portisi, a possible Balaenoptera, the new species Balaenoptera bertae, and two right whales (Eubalaena spp.). Curiously absent from the fossil assemblage are tusked odobenine walruses and beluga-like monodontids (both present in other Pliocene sections of the Purisima, and will likely be found after further sampling) and hydrodamaline sirenians (e.g. Hydrodamalis cuestae), also absent from other Pliocene sections of the Purisima but abundant in coeval rocks further south in California, as well as basal late Miocene strata of the Purisima. Sirenian bones have an extraordinarily high preservation potential thanks to their large, pachyosteosclerotic (super dense) bones, and the complete absence of their fossils amongst hundreds of other marine mammal fossils suggests that this is a true absence, as their absence cannot really be argued from a taphonomic perspective. In other words, the same biases exist against other marine mammal groups, and even in intense taphonomic conditions sirenian bones are still just as common - if not more common - than cetacean bones.

The curious thing about this assemblage is that it shows that the marine mammal fauna of the Pliocene North Pacific was quite a bit different from the modern fauna. It includes numerous archaic species, such as "Balaenoptera" portisi, Herpetocetus, and a delphinid-like porpoise with a primitively asymmetrical skull, marine mammals with strange adaptations such as the as-yet unnamed "skimmer" or "half-beaked" porpoise with the elongate, edentulous "chin" that protruded beyond the upper jaw, the double-tusked walrus Dusignathus, and Herpetocetus (which counts again in this category as it had a strange feeding apparatus adapted for benthic filter feeding). The remaining marine mammals include species that are far removed with respect to modern relatives, such as Parapontoporia, the sister taxon to the recently extinct Yangtze river dolphin (Lipotes), and beluga-like monodontids and tusked odobenine walruses such as Valenictus (with modern relatives now restricted to the arctic), and early species within modern lineages, such as the newly described Balaenoptera bertae, the fur seal Callorhinus gilmorei, and an early harbor porpoise, Phocoena sp. (the Cuesta sea cow, Hydrodamalis cuestae, also counts towards this as it is known from other localities and is an early record of the recently extinct Steller's sea cow, Hydrodamalis gigas).

What explains the persistence of such a strange fauna, while modernized marine mammals were already abundant in the Atlantic? A warm-water equatorial barrier lay to the south, with the recently closed Panamanian isthmus to the east; the Bering strait had not yet opened, restricting dispersal to (and from) the north. After the Pliocene, climatic deterioration and associated oceanic cooling permitted dispersal across the equator, and the Bering strait opened up, allowing marine mammals to disperse through the arctic.

Life restoration of Balaenoptera bertae, a Pliocene species of rorqual from the Purisima Formation of Northern California. Artwork by RW Boessenecker.

Read more:

Official University of Otago Press Release. February 6, 2014.

Strange marine mammals of ancient North Pacific revealed. Science Daily, February 6, 2014.

Dwarf whales, twin-tusked walrus once swam West Coast., February 7, 2014.

Otago student's whale of a find. Otago Daily Times, February 7, 2014.

Balaenoptera bertae: new fossil whale species discovered. Sci-News, February 7, 2014. 

Fossils reveal eclectic ancient marine mammals of North Pacific. Redorbit, February 7, 2014.

Fossils show strange marine mammals lived in pre-Ice Age Pacific., February 6, 2014.

Pre-Ice Age whale found. Radio New Zealand, February 6, 2014.

Kiwi's key to ancient seas. New Zealand Herald, February 7, 2014.

New species of fossil whale excavated from San Francisco Bay Area's Purisima Formation. Science, Space, and Robots, February 6, 2014.

And of course, there's the original peer-reviewed article too:

Boessenecker, R.W. 2013. A new marine vertebrate assemblage from the Late Neogene Purisima Formation in Central California, Part II: Pinnipeds and Cetaceans. Geodiversitas 35:4:815-940.