Monday, January 14, 2013

Sinus anatomy of modern porpoises revealed by CT imaging

Congratulations are in order to my colleague and friend Rachel Racicot, a Ph.D. student at Yale (working under Jacques Gauthier), for getting her master's research published in the Journal of Morphology. Rachel did her Master's at San Diego State with Annalisa Berta, and was just finishing up when I visited the San Diego NHM for the first time in 2007. Aside from functional morphology and the endocranial anatomy of odontocetes (particularly cranial sinuses, brain endocasts, and the inner ear), Rachel is also interested in fossil porpoises and is currently researching the strange "half-beaked" porpoise from the San Diego Formation. Rachel's master's research concerns the pterygoid sinus morphology of modern porpoises.

Ms. Racicot had no idea that the journal had selected her image to be put on the cover 
of the January 13 issue, and she was quite surprised when I congratulated her on it. Pleasantly 
surprised, I should say.

Before I continue, I should briefly introduce phocoenids. The Phocoenidae, or true porpoises, are a small bodied group of delphinoid cetaceans that are not terribly diverse (6 species, 3 genera) in comparison to oceanic dolphins (Delphinidae; ~40 species, ~12 genera). They differ from delphinids in having short rostra, having symmetrical skulls, large bumps on the premaxillae just before the bony nares, and have inflated braincases without large bony crests. Phocoenids are considered to be paedomorphic -that is, retaining juvenile features into adulthood, thus explaining A) their inflated, juvenile-like braincases, B) lack of strong bony crests, C) cranial symmetry, D) short rostra, and E) small body size. It should be noted that the delphinid Cephalorhynchus is thought to parallel phocoenid paedomorphosis. Modern phocoenids also have strange, spatulate teeth which almost resemble the teeth of nodosaurs and ankylosaurs. Many fossil phocoenids, on the other hand, have longer rostra, conical teeth, cranial asymmetry, and better developed cranial crests.

Schematic view of a neonatal harbor porpoise (Phocoena phocoena) skull showing in blue the various parts of the pterygoid sinus. From Racicot and Berta (2013).

The pterygoid sinus is present in all Neoceti, and even within basilosaurids. It originates as an outpocket of the eustachian tube (an air filled cavity present in the middle ear of all mammals - hold your nose with your fingers and blow, and you'll feel crackling in your eustachian tubes; they are also what "pop" when changing altitude as the pressure changes). Parts of the sinus system can be seen externally, such as the hamular lobe of the pterygoid sinus, which is not completely encased in bone and is visible in a prepared skull as large cavities surrounded by thin flanges of bone. The pterygoid sinus system is elaborated in odontocetes relative to mysticetes. Although known to exist, the anatomy of the pterygoid sinus system in odontocetes - and true porpoises (Phocoenidae) in particular - is difficult to assess. Since they are cavities within a solid object, it's difficult to study them by any conventional means as they remain hidden in the skull. Certain aspects of the pterygoid sinuses have, for example, been used in phylogenetics - in multiple phylogenetic analyses which have included phocoenids, a cladistic character has been used - presence or absence of a dorsal extension of the preorbital lobe of the pterygoid sinus between the maxilla and frontal bone (po on the above diagram). This is a phocoenid feature, and the bottlenose dolphin lacks this. The preorbital lobe is well developed in the neonatal specimen (neonate = newborn individual, rather than a juvenile or subadult), although the dorsal extension is not as well developed as in the adults (an example of ontogeny recapitulating phylogeny).

Digital 'endocast' of the right pterygoid sinus (in medial view) from six skulls of Phocoena phocoena; anterior is to the left. Neonate specimen shown in F. The sinus shape looks pretty weird (but then again, so does the rest of a cetacean skull). From Racicot and Berta (2013).

 So, what's it for? Previous hypotheses for the function of the sinus includes A) an acoustic barrier to reflect sounds produced during echolocation forward through the melon, B) an acoustic barrier between sound producing and sound receiving structures (e.g. nasal region and petrotympanic complex, respectively), and C) to acoustically isolate the petrotympanic complex from sounds produced during echolocation (which, admittedly, sounds similar to B). A fourth hypothesis posits that the pterygoid sinus serves as a means to regulate pressure around the middle ear during diving.

 The paired sinuses (right and left) of Phocoena phocoena specimens in anterior view. Note that there is right-left asymmetry in each specimen. From Racicot and Berta (2013).

To test the sound reflecting ability of the sinus, Racicot and Berta calculated the minimum thickness necessary to reflect sound at the typical highest frequency sounds produced by Phocoena phocoena (~150 kHz). Many aspects of the cetacean skull make sense in the light of acoustic impedence - sound waves tend to bounce off of objects or features where there is a stark change in density. For example, echoes in air are sound waves bouncing off a solid surface. In water where the medium is much denser, sound not only travels faster, but flesh and bone are so similar in density that sounds travel through the vertebrate body rather than bouncing off of it - making things like external ears (which take advantage of sound waves bouncing due to acoustic impedence, and funnels sound in) useless. So, within a skull, a wall of air within a sinus is different enough in density to reflect sound, analogous to a solid object in air.

They calculated that the preorbital lobe would need to be 2.5mm thick at a minimum, which is less than what they observed in phocoenid sinuses - indicating they would function well at reflecting sounds. As for the asymmetry of the sinuses, they remarked that this could be explained by the fact that experiments have determined that porpoises produce sounds in an asymmetric fashion, preferring to use one nasal passage over the other, potentially explaining why the sinuses are asymmetrical.

Wild speculation time: it's also possible that aysmmetrical sinuses may be a vestige of cranial asymmetry. Fossils show that the earliest phocoenids had asymmetrical skulls in a similar fashion to delphinids; perhaps this is an example of phylogenetic inertia - the external skull changed at a faster pace than the sinuses, reaching symmetry first. However, paedomorphosis typically progresses by delaying adult morphology later and later during ontogeny, and retaining juvenile features longer and longer instead. In other words, paedomorphosis would suggest that asymmetry was once an adult feature which at some point was lost because juvenile symmetry prevailed - which doesn't totally jive with asymmetrical sinuses being retained, unless the two are decoupled somehow, progressing along different ontogenetic trajectories. Or, is asymmetry so ingrained within odontocetes that it's a juvenile feature in phocoenids, with symmetry really being secondarily gained via hypermorphosis, with asymmetry being pushed earlier on in ontogeny? Interesting questions, but they remain unanswered. We need more fossils and further studies of modern phocoenid cranial anatomy.

Another last thought - it's interesting to note that phocoenids are considered paedomorphic, but have relatively extensive pterygoid sinuses. The primitive condition among Neoceti, of course, is possessing less well developed sinuses (pterygoid sinuses in Neoceti and Basilosauridae are acquired stepwise in a piecemeal fashion). In other words - sinus development is not showing a paedomorphic trend - in fact, it's showing the opposite trend - it's a peramorphic feature, probably undergoing something like hypermorphosis (development is postponed and extended later into ontogeny) or acceleration (faster development of a feature during ontogeny). Perhaps hypermorphosis is not likely, given the short period it takes for phocoenids to mature.


Racicot, R.A., A. Berta. 2013. Comparative Morphology of Porpoise (Cetacea: Phocoenidae) Pterygoid Sinuses: Phylogenetic and Functional Implications. Journal of Morphology 274:49-62.

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