The Whale That Walked: A Broad Overview of Morphological and Adaptive Change In Cetaceans From Pakicetus to Mysticetes
After a bolide collision at the end of the Maastritchtian period caused the catastrophic extinction of dinosaurs, most ecological niches occupied by terrestrial and aquatic megafauna were left open to fill. These areas, dominated by dinosaurs and marine reptiles since the early Jurassic became filled by mammals, who were present since the Carnian period of the Upper Triassic. One of these niches left open was in the Eocene seas, where the extinction of aquatic squamates such as Mosasaurs and Plesiosaurs vacated positions for apex predation. The Eocene period ranged from approximately 56 - 33.9 MA, and was a period of extreme global warming, an event known as the Paleocene-Eocene Thermal Maximum, that occurred from approximately 55.8 MA – approximately 170,000 years ago. With no ice caps present at either pole, sea levels were high, leading to more coastal, brackish water environments. These environments were the home of the common ancestors of modern cetaceans, which have undergone a dramatic change in morphology to move from terrestrial creatures into the obligate aquatic animals we observe today.
The basal cetacean fossil record is minimal and most of the specimens have been discovered in the Kashmir region of Northern India (Cambay Shale Formation) and Pakistan (Kuldana Formation) which was a marine straight environment, with braided, brackish fluvial deposits that infer a tropical, shallow marine contact with fresh water streams. This was a faunally diverse ecosystem that allowed many successful mammals to thrive, such as creodonts, brontotheres, perissodactyls, artiodactyls, chiropterans, proboscids, sirenians, and primates (Gingerich, et al. 1983). But our story begins with Pakicetus, a small, amphibious mammal that lived approximately 53 million years ago along the coast land of the closing Tethys Sea and how its basal cetacean morphology would transform into creatures such as Balaenoptera musculus, the largest creature that has lived on Earth.
On the surface, Pakicetus was not unlike most terrestrial mammals of the Eocene. It was a quadruped with a body shape that was akin to hoofed mammals and is the only basal cetacean belonging to the sub-order Archaeoceti that had long, fully functional legs. Based on cranial specimens, the animal is thought to be between 3.3 and 6.6 feet in length, with a long snout, flexible neck, and a long robust tail. The nasal openings were located at the end of the snout, but the eyes were located closer to the top of the skull, not unlike crocodilians, who ambush their prey from below (Thewissen, et al. 2001).
The habitat of Pakicetus has been a topic of debate for some time, with some believing a fully terrestrial mode of life, while most research points to a semi- aquatic one. The location of the orbits on the top of the skull is one indication of its potentially semi-aquatic habitat and this morphology is common in aquatic animals that live in water but look at surface objects (Thewissen, et al. 2009). Another argument for the semi-aquatic habitation is the hind leg bones are osteosclerotic, which due to their increased density, provide ballast and possibly allowed the animal to float motionless while immersed (Thewissen, et al. 2009). Another cetacean-like morphological distinction is in the skull, which shows a large auditory bulla, which in cetaceans is formed from the ectotympanic bone only, as opposed to the tympanic bone in most mammals (Gingerich, et al. 1981). This is a specialization for underwater hearing and in extant cetaceans, is usually accompanied by a large mandibular foramen in the lower jaw that would contain a fat pack extending towards the ear allowing them to “hear” underwater. Pakicetus is the only basal cetacean besides Indohys that is missing the fat pack, but has an enlarged auditory bulla, inferring that these two species are ancestors to modern cetaceans (Thewissen and Hussein 1993).
The next morphological adaptations that point towards a more aquatic habitat in the fossil record are from an archaeocetid named Ambulocetus natans, which lived 43.3 MA in what is now Pakistan. During the Eocene, Pakistan was a coastal region near the encroaching Deccan plateau which was an large island in the Tethys Sea. Ambulocetus was slightly more adapted to a fully aquatic lifestyle, although was probably still semi-aquatic, spending most of its time in water. In comparing Ambulocetus and Pakicetus, which are separated by 5 million years, we see an increase in size from a maximum proposed size of 6.6 feet in Pakicetus to 10 feet in Ambulocetus (Gingerich 2003).
Ambulocetus was probably a uniquely ugly creature, looking like a crocodilian otter with patchy fur. A postulated hunting strategy is similar to crocodilians. With its hind limbs adapted for swimming, the creature could wait in the shallows and ambush passing animals from below. This semi-aquatic hunting strategy was accompanied by a new adaptation in the fossil record that indicates a change in the nose that allowed the animal to swallow underwater. Other morphological changes present in Ambulocetus and not Pakicetus or Indohyus is the fat pad in the jaw. Ambulocetus lacked external ears and in order to “hear” prey on land, would lower its jaw to the ground to detect vibrations which would travel along the jaw and vibrate the fat pad. In water, its periotic bones resemble a primitive version of cetaceans giving it the ability hear underwater (Thewissen and Hussein.1993). The dentition begins to change with this specimen as well, showing a more cetacean like tooth differentiation and chemical analysis has shown that they lived in both marine and limnic environments (Thewissen, et al. 1996).
While the previous specimens are presumed to be semi aquatic, between 49 and 40.4 MA there appears to be an archaeocetid influx into the marine niches that have been long absent since the marine reptiles went extinct. Two of these genera, Kutchicetus and Rodhocetus, show a transition from a semi aquatic, fresh/brackish lifestyle to a fully marine lagoonal environment that led to further morphological adaptations to suit this environment change.
Kutchicetus existed in the same geography and paleoenvironmental context as Ambulocetus, but lived for about 2 million years longer. It was during this time that fossils found have shown a full adaptation to a marine environment. This is evident by the lithofacies the specimens were found in, which indicate a shallow marine environment that was near shore and likely lagoonal (Thewissen, et al. 1996). It is at this stage in ceteceans development that we see archaeocetids that have gained the ability to ingest salt water, displaying a full transition to a marine environment (Thewissen, et al. 2009). Saltwater and freshwater have different ratios of oxygen isotopes and using isotopic analysis on the teeth and bones show that Kutchicetus likely drank both saltwater and freshwater. Whales that evolved after Kutchicetus show even higher levels of saltwater oxygen isotopes, indicating that they lived in nearshore marine habitats and were able to drink saltwater as today's whales can. Some of the morphological changes that occurred alongside the marine transition were equally important. The orbits were still on the top of the skull, but have reduced significantly, indicating a reduced need for vision in hunting. The semi-circular canal, a structure containing fluid located in the inner- ear, was reduced in size. It is responsible for maintaining balance in terrestrial mammals, a function no longer needed for stalking prey in the nektonic zone of the sea (Spoor, et al. 2002). The limbs of Kutchicetus were greatly reduced in size compared to Ambulocetus and there is also a distinct change in the spine and hips as well. It had a strong tail and had four fused sacral vertebrae articulated to the hip for aquatic locomotion (Bajpal and Thewissen.2000). It is assumed the animal moved through the water by caudal undulation, with its tail being used to steer as a rudder. While blubber had not developed yet, there is evidence the animal was completely covered in fur. Kutchicetus was a diminutive archaeocetid, measuring 8 feet and probably weighing about 100 lbs. (Spoor, et al. 2002).
While the previous 4 mentioned genera belonged to the sub-order Archaeoceti, a new family arose about 45 million years ago; the Protocetidae. The first Protocetids were a family of very whale-like, semi-aquatic predators with very different morphological adaptations to sea life than the previously discussed specimens. It is believed Protocetids were the first cetaceans to spread from the Tethys to the oceans of the world (Gingerich. 2003). While there are multiple branches on the Protocetal tree, I will focus on one genus in particular, Rodhocetus.
Rodhocetus lived about 48 to 40.4 MA in the same facies as Kutchicetus, but displays a more cetacean appearance. Its orbits were much larger than previous specimens and had migrated from the top of the skull to a lateral position, indicating the days of crocodilian ambushing strategies were over. This enabled them to hunt with greater success in the water, inferring less and less time was being spent on land. A protocetid named Maiacetus was found with a fossilized fetus inside the womb with its head facing downward suggesting they still gave birth on land (Gingerich, et al. 2009). The nasal openings have migrated as well, moving halfway up the snout and increasing in size. I surmise this was the beginnings of modern breathing behavior in cetaceans, with the animal not having to face upward to get air. The ability to hear underwater was further adapting as well, with an increase in the size of the mandibular foramen and the auditory bulla, but a still present auditory meatus which is absent in modern whales. This shows an intermediary stage in the development of cetacean hearing and most likely whales in general. This animal probably looked like a bizarre whale-pig, with a large cetacean skull, short limbs that ended in webbed hooves and dorsally covered in hair. While its limbs seem adapted to underwater paddling, they are a poor design for walking on land and it is hypothesized that they moved awkwardly, similar to modern Pinnipeds (Gingerich, et al. 2009). This would be the last stage in the cetacean line that resembled a terrestrial animal.
Approximately 40-34 MA in the period of the Middle to Late Eocene lived a dispersed, fully marine genus Basilosaurus. The first thing that stands out to me was the size of the animal. In Rodhocetus, we see a size of 10-12 feet and 900-1000lbs., but Basilosaurids have been measured to reach such lengths as 65 ft.(Gingerich, 2003)! A massive creature, it would have been the largest animal alive at the time and the largest known apex predator of the Eocene. The diet of Basilosaurus is known to have consisted primarily of flesh, with the stomach contents of different species of Basilosaurs showing a diet exclusively of sharks, fish, and other whales. Studies on the dental wear shows mastication occurred prior to swallowing (Gingerich and Uhen, 1998) and Basilosaurus showed similar feeding patterns to modern cetaceans. Fossilized stomach contents discovered in two different species on opposite sides of the world show one species diet consisting of sharks and fish while the other shows a diet consisting of Dorudon, another prolific protcetid of the time. This is similar to prey preference shown in modern Orcas that live in different regions (Fahlke, 2012).
In Basilosaurs, we see further morphological changes in the skull related to multi-directional hearing and sound production. At this point in cetacean evolution there is an asymmetry in the skull morphology that is associated with creating high frequency sounds used in echolocation, a function that had yet to manifest in Basilosaurs despite the skull beginning to show asymmetry (Fahlke et al. 2011). The sinuses are primitively cetacean, with the bones arranged in a way to be filled with air. This allows the creature to isolate audio waves in the dense medium of the sea and is not present in prior Archaeocetids (Numella et al. 2004). The nasal opening has migrated closer to the present position ( not yet a “blowhole”) and the hind limbs have reduced greatly. One postulation regarding the stunted hind limbs is that they were used in mating. Given the size of Basilosaurs and anatomical models derived from bone morphology, it is assumed mating was a dangerous and awkward process given the environment of the open sea. Therefore it is theorized that the tiny hind limbs would interlock with the partners during copulation. This would stabilize the creatures in a vertical – vertical caudal position. The fact that the size of the limbs is so reduced and that they were fused to the sacral vertebrae indicate locomotive use was unlikely (Bedjer and Hall, 2002). One final morphological development in Basilosaurids was the tail and the emergence of tail flukes to aid in locomotion. Basilosaurus had a small primitive fluke that would have probably allowed the animal to navigate vertically. It is postulated that they moved in a way quite differently than modern cetaceans, adopting more of an anguilliform movement pattern, which is a side-to- side motion as opposed to the vertical undulating motion of modern cetaceans. It is also believed that Basilosaurus was fully marine and never ventured on to land (Gingerich and Uhen, 1998).
Continuing through time, cetaceans eventually branch into the two modern sub-orders that all extant cetaceans belong to; Odontocetes (toothed whales) and Mysticetes (the baleen whales). There are distinct differences that evolved over time to differentiate the two from each other. In Odontocetes, there are echolocation and a pronounced rostrum, while Mysticetes displays adaptations in the skull and jaw for filter feeding and baleen.
Echolocation is a means of communication by sonar and is used by chiropterans, cetaceans, shrews, and a few species of birds. Sound is emitted by the animal into the surrounding environment and the echoes of those sounds reflecting off of objects return to the animal as “images”, allowing them to discern objects. In Odontocetes, it is advantageous due to the turbidity and low light found in the oceans and also because the dense medium of water is acoustically superior than air in its ability to transmit sound (Morisaka and Connor, 2007). The mechanism by which echolocation works in extant cetaceans is a complex reflection system based on the mandibular foramen in combination with a “melon organ”, a unique feature only to odontocetids. The melon organ is a large mass of tissue located in front of the cranium that sits between the blowhole and the rostrum and is considered to be associated with the nasal cavity. It is comprised of a dense waxy tissue that acts as a good reflector of acoustic vibration and sound, giving the animals the ability to direct sound intentionally. The first evidence of this is shown in the Burdigalian stage of the early Miocene species Squalodon which lived approximately 16 million years ago. While fossil specimens are minimal, the skull is mostly complete and shows cranial distortion in the forehead where the melon organ rests, albeit not as dramatic as in extant cetaceans. This infers the possibility of an early stage in development of the melon organ and echolocation (Mchedlidze, 1984). Squalodon also exhibits other commonalities with modern Odontocetes. Its nasal openings have shifted to near modern position and merged into a single nasal opening that is assumed to be a blowhole while the hind limbs are now internalized, although structurally dwarfed and intact.
In Mysticetes, there have been major morphological changes in the jaw and skull to accommodate not only physical adaptations, but behavioral adaptations as well. Mysticetes are in their own sub-order because their dentition has evolved into a bristly and filamentous material know as baleen. Baleen is used specifically for filter-feeding and can vary in size within species, but is always used for feeding. As the whale intakes large amounts of water into its gaping mouth, it then expels the water through the baleen which filters out small creatures such as krill, small fish , and copepods . It is unclear when exactly baleen evolved, with paleontologists assuming an age of approximately 30 million years ago. Baleen is problematic to paleontologists because it is a poor substance for fossilization and the oldest fossilized baleen dates to approximately 15 million years ago, but certain morphological changes in the skull and jaw in transitional species lead paleontologists to believe the divergence was older. Some of these changes to the dentition include specimens that had peripheral teeth as well as baleen, as evidenced by mechanisms providing blood flow in the jaw along with buttressing of the bones in the upper jaw below the eyes. Another modification in the lower jaw was the Mandibular rami only attached to each other by a ligament (at the symphysis) (Deméré, et al. 2007). It is unclear why baleen feeding evolved, but there are some theories that address this. One theory is that during this time the earth had begun to cool and was changing from a “greenhouse” world to an “icehouse” with the oncoming ice age of the Neogene. This would have changed ocean currents gradually as Antarctica began to glaciate resulting in a variety of pelagic habitats and increased partitioning of food resources.
I feel that whales are an important example of evolution not only because they have returned to the water, but their synapomorphic traits for adapting to this environment differ from fish. While cetaceans share the same generalized structures for locomotion as fish, they are very different, yet as efficient . This is exciting to me because it shows that nature will always find a way to exploit niches and resources. In cetaceans, the marine niche of apex predation was able to be occupied after the K/T extinction due to the extinction of marine squamates and there is a period of 13 million years where sharks were the dominant predators until cetaceans moved into marine environments. I was also pleased to find that the fossil record for the transitional morphs was quite rich and look forward to researching other species and their origins. It is a matter of debate which order whales belong to, notably between Mesonychids and Artiodactyls, and the matter deserves many papers focused on that. Recent studies have shown that ankle bone fossils in Rhodocetus are more closely related to artiodactyls due to them both sharing the same astragalus “double pulley” heel bone system (Thewissen and Madar 1999).
- Gingerich, Philip D.; Wells,Neil A.; Russell, Donald E.; and Ibrahim Shah,S. M.(1983) “Origin of Whales in Epicontinental Remnant Seas: New Evidence from the Early Eocene of Pakistan” : Science, New Series, Vol. 220, No. 4595 , pp. 403-406
- Thewissen, J. G. M.; Williams, E. M.; Roe, L. J.; Hussain, S. T. (2001).“Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls” Nature 413 (6853): 277–281
- Thewissen, J. G. M.; Cooper, Lisa Noelle; George, John C.; Bajpai, Sunil (2009)."From Land to Water: the Origin of Whales, Dolphins, and Porpoises" Evolution: Education and Outreach (2): 272–288.
- Gingerich, Philip D.; Russell, Donald E. (1981)."Pakicetus inachus, A New Archaeocete (Mammalia, Cetacea) from the Early-Middle Eocene Kuldana Formation of Kohat (Pakistan) Contributions from the Museum of Paleontology, The Museum of Michigan 25( 11): 235–246.
- Thewissen, J.G.M.; Hussain, S.T. (1993)."Origin Of Underwater Hearing In Whales" Nature 361 (6411): 444–445.
- Thewissen, J. G. M. and Madar, S. I. (1999)“Ankle Morphology of the Earliest Cetaceans and Its Implications for the Phylogenetic Relations among Ungulates” : Systematic Biology, Vol. 48, No. 1 , pp. 21-30: Oxford University Press for the Society of Systematic Biologists
- Ursing, Bjorn M. and Arnason, Ulfur (1998)“Analyses of Mitochondrial Genomes Strongly Support a Hippopotamus-Whale Clade” Biological Sciences, Vol. 265, No. 1412, pp. 2251-2255P: The Royal Society
8. Gingerich (2003)“Land-to-Sea Transition in Early Whales: Evolution of Eocene Archaeoceti (Cetacea) In Relation to Skeletal Proportions and Locomotion of Living Semiaquatic Mammals ” Paleobiology, Vol. 29, No. 3 , pp. 429-454
9. Thewissen, J. G. M. and Williams,E. M. (2002)“The Early Radiations Of Cetacea (Mammalia): Evolutionary Pattern and Developmental Correlations” Annu. Rev. Ecol.Syst. 2002. 33:73–90
10. Thewissen, J.G.M.; Madar, S.I.; Hussain, S.T. (1996).“ Ambulocetus natans, an Eocene cetacean (Mammalia) from Pakistan.” Courier Forschungsinstitut Senckenberg 191. pp 1–86
- Spoor, F.; Bajpai, S. Hussain, S. T., Kumar, K., Thewissen, J. G. M. (2002)"Vestibularevidence for the evolution of aquatic behaviour in early cetaceans" ..Nature 4176885): 163–166.
- Bajpai, Sunil; Thewissen, J. G. M. (2000)."A new, diminutive Eocene whale fromKachchh (Gujarat, India) and its implications for locomotor evolution" . CurrentScience 79 (10): 1478–82.
- Gingerich PD, ul-Haq M, von Koenigswald W, Sanders WJ, Smith BH, et al.(2009)"New Protocetid Whale from the Middle Eocene of Pakistan: Birth on Land, Precocial Development, and Sexual Dimorphism". PLoS one.
- Gingerich, P. D.; Uhen, Mark D. (1998). "Likelihood estimation of the time of origin of Cetacea and the time of divergence of Cetacea and Artiodactyla". Palaeontologia Electronica 1 (2): 1–45.
- Fahlke, Julia M.; Gingerich, Philip D.; Welsh, Robert C.; Wood, Aaron R. (2011) "Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water". PNAS 108 (35)
- Nummela, Sirpa; Thewissen, J. G. M.; Bajpai, Sunil; Hussain, Taseer; Kumar, Kishor (2004). "Eocene evolution of whale hearing". Science 430: 776–778
- Bejder, Lars; Hall, Brian K. (2002). "Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss". Evolution and Development 4 (6): 445–458.
- Fahlke, Julia M. (2012). "Bite marks revisited – evidence for middle-to-late Eocene Basilosaurus isis predation on Dorudon atrox (both Cetacea, Basilosauridae)". Palaeontologia Electronica 15 (3)
- Morisaka, T., and R.C. Connor, (2007). "Predation by killer whales (Orcinus orca) and the evolution of whistle loss and narrow-band high frequency clicks in odontocetes." Journal of Evolutionary Biology 20:1439-1458.
- Mchedlidze G.A.; Translated by Chakravarthy, R. (1984). “General Features of the Paleobiological Evolution of Cetacea”. New Delhi: Oxonian Press.
- Deméré, Thomas; Michael R. McGowen, Annalisa Berta, John Gatesy (2007). "Morphological and Molecular Evidence for a Stepwise Evolutionary Transition from Teeth to Baleen in Mysticete Whales". Systematic Biology 57 (1): 15–37.