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
No comments:
Post a Comment