Course:BIOL250/The Evolution of Cetaceans

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A cladogram of cetaceans and their relative families.

Overview of Cetacean Evolution

Cetacea

North Atlantic Right Whale mother and her calf, examples of the suborder Mysteceti

The Order Cetacea is a group of carnivorous marine mammals, which include dolphins, porpoises and whales. Living in waters all over the world,the order Cetacea inhabit the widest range of the planet out of any other order in the animal kingdom. Today Cetacea include over 80 species including the largest living animal Belaenoptera musculus (the blue whale). The order Cetacea can be classified into two different suborders, the Odontoceti and the Mysticeti. The suborder Odontoceti includes dolphins, porpoises, belugas, narwhals, and other toothed whales. They are characterized by their smaller size, single blowhole, and their feeding strategy using teeth and echolocation. The suborder Mysteciti (also known as the baleen whales) includes the larger filter feeding whales such as blue whales, humpback whales and right whales.

Evolution: From Land to Water

There are several morphological and behavioral characteristics shared by the order Cetacea that suggest these large marine mammals share a terrestrial common ancestor. Evolution of Cetacea from terrestrial mammals is evidenced by their need to surface from the water to breathe air; the bones of their fins, which closely resemble the limbs of land mammals, the presence of hairs in the fetus of some Cetacea species, and the vertical movement of the Cetacea spine, representative of a running movement more so than the movement of a fish through water[1]. Although the morphological evidence was present, it wasn't until the past two decades, and several fossil discoveries in India and Pakistan that the pattern of descent of the cetacea began to take shape.

It is commonly believed that the evolution of ancestral cetaceans from terrestrial to marine life was accompanied by a rapid morphological adaptation [2]. The traditional theory of the evolution of cetaceans suggests that modern whales are descendants from ungulate wolves, belonging to the ungulate order known as Artiodactyla. From this group, a species known as the Indohyus is believed to be the earliest known ancestor of the order cetacea. Recent evidence from the University of California- Berkley suggests that the whale’s closest living relative is the hippopotamus[3].

Phylogenetic tree showing ancestry of modern cetacea

Eocene epoch

The start from the transition from land to water is believed to have started with the Pakicetus, a small, dog-like animal often considered to be the “first whale”. The anatomy of the Pakicetus middle ear bone is the distinguishing feature that puts it at the beginning of the root of whale evolution [4]. From the Pakicetus, we see the evolution into a more aquatic ancestor known as the Ambulocetus. The Ambulocetus was known as the “walking whale” and showed evidence of adapting to more of a marine lifestyle. Fossils records suggest that this was the next step in the evolution of cetaceans as the hands were more enlarged (like flippers) and the tail was larger and more muscular[4]. The genus Remingtonocetidae is the next step in the lineage, and is characterized by it's long snout. The Remingtonocetidae fossil records show that this may be the first genus where the modern cetacea's stiff, immobile neck first developed, as well as the large sensory "balance" organ, which comes with the more specialized ear anatomy[1]. The Protocetus is known as the genus of whale lineage that shows the first evidence of blowhole formation. Fossil records show the movement of the Protocetus nostrils moving further up to the top of the head, evidencing the early formation of what would become the blowhole[4] . By the late eocene epoch, the largest ever known genus of whales evolved, known as the Basilosaurus, a slightly inappropriate name, as it was a mammal, not a lizard. The Basilosaurus was a particularly important step in the evolution of modern cetaceans, as it was the first to demonstrate the large size and fully aquatic lifestyle. Basilosaurids and the closely related genus Dorudontids had a very similar skull morphology, causing them to sometimes be grouped together in one family (basilosauridae). Both had short necks and overall skull morphology similar to modern cetacea [5].

Modern Cetacea

By the late Oligocene, Aetiocetus had evolved. It had skull and jaw features typical of baleen whales, and is considered to be the earliest mysticete. By the late Miocene epoch, whales of both Myteciti and Odontoceti lineages are relatively common fossils in many marine deposits [6]. Although both Mysticeti and Odontoceti show common ancestry, the two sub-orders (together known as the Neoceti) evolved two very different feeding and huntinch mechanisms. The Odontoceti evolved the ability to hunt through echolocation, which reflects sound waves off surrounding objects, while the Mysticeti use a process known as filter feeding, which uses baleen plates in their mouths to feed on bulk prey (e.g. krill)[1].

Musculoskeletal Evolution

Overview

The group of species that would become the cetacean family underwent a remarkable history of change throughout their 60 million-year history. Beginning as small, even-toed hoofed members of the artiodactyl family [7], they rapidly diverged from their land-dwelling relatives and adapted for aquatic life, undergoing radical physiological adaptation to their new aquatic habitats in an evolutionarily-short period of time; hoofed limbs atrophied or became flippers, muscles shifted in size and position to accommodate an axial swimming pattern and features like fur dissipated in favour of blubber and fine vellus hair. [8]

Flippers and Hind Limbs

Perhaps the most dramatic change emerged in the limbs of the cetaceans, whereby hooves evolved to become either elongated paddle-like flippers or atrophy away completely, in the case of hind limbs. It is likely that the evolution towards flippers began very early in the cetaceans' path to an aquatic lifestyle and arose as a result of directional selection pressure towards better swimming capabilities in the artiodactyl-like proto-cetaceans. [8] Early cetaceans like Ambulocetus natans, which lived in the early Eocene (50 to 48 mya) in what is now Pakistan, demonstrate this early phenotypic adaptation, with powerful back limbs and large, likely-webbed feet with flat toes, facilitating the earliest forms of the rapid, up-down swimming pattern which would come to characterize cetaceans in the later fossil record. [9] Early cetaceans like A. natans would have had a limited ability to move about on land, but later species would gradually lose this ability entirely as their limbs became adapted to a full-time aquatic lifestyle. [8]

As cetaceans began to take to aquatic environments on a more permanent basis, the motility and strength of the forelimb atrophied over time due to its lack of utility to the primary swimming motion. [8] The motility of the forelimb's digits were first to be lost, fusing into a recognizable paddle-like shape, and were quickly followed by rapid shortening of the forearm and arm itself. Rodhocectus, a late transitional cetacean which lived in the middle Eocene (~47 mya), demonstrates this shortening and specialization of the forelimb as well as the consequent strengthening of the vertebral swimming musculature and gradual decrease in motility of the hind limbs as their movements became more specialized.[8]

Over time, the hind limbs would both decrease in mobility as well as size , shrinking down as the fluke, which originated as a spur of connective tissue in the tail, took precedence in aiding the swimming power of the vertebral muscles. In the late Eocene cetaceans Basilosaurus and Dorudon (30-40 mya)¸ the hindlimbs had atrophied almost to the point of vestigiality, and likely only functioned as an aid in copulation by grasping the whale's partner. [8]

The emergence of the fluke, the specialization of the forelimb and the atrophication of the hindlimb by the time of Basilosaurus in the late Eocene marked the end of the major evolutionary pressure towards phenotypic variation in the limbs and flukes of whales, but also marked the beginning of the cetaceans' expansion into new ecological niches and thereby development of new traits elsewhere in their anatomy.

Vertebrae, the Pelvis and the Caudal Fluke

The vertebrae and spinal column, as well as the pelvis of cetaceans underwent significant changes throughout their evolutionary history as well, if not to quite as dramatic a degree as the limbs of the organisms. As cetaceans adapted to a full-time aquatic lifestyle, they became more and more dependent on their ability to swim proficiently, which was highly dependent on the muscles in the lower vertebral column and tail. As such, the cetaceans underwent a period of evolutionarily-rapid selection for powerful dorsoventral muscles, which, consequently, drove a decline in side-to-side motility in those vertebrae, and even fused some together even as evolutionary pressure drove the development of a long, muscular tail via the development of more and longer vertebrae. [10]

The development of the tail fluke, which is ubiquitous among living cetaceans, likely arose out of strong directional selection operating on a mutation that governed the growth of a spur of connective tissue, driving it to expand and increase in rigidity at an evolutionarily-rapid rate until it attained a relatively modern form in the basilosaurids and rorudontids. [11]

Specialization and Niche Exploitation

As cetaceans adapted to an aquatic lifestyle they quickly diversified, moving into new ecological niches and habitats that were left vacant after the extinction of the dinosaurs and most marine reptiles during the Cretaceous-Tertiary boundary extinction event 65 mya.

Most early cetaceans were predators, catching fish and molluscs by means of their powerful swimming muscles and sharp teeth, but as the cetacean superfamily diversified and multiplied, many cetacean groups adopted different niches. Basilosaurus, for example, likely evolved to hunt and eat other marine mammals, including other cetaceans, as evidenced by fossils of Dorudon calves with Basilosaurus-linked bite marks indented in the bones.

Most remarkably, however, a group of whales now known as the mysticetes began to evolve to take advantage of a remarkably different niche; beginning with the late Oligocene (~ 25 mya) whale Janjucetus, highly-specialized structures known as baleen began to appear in the fossil record, presumably developed as a means of catching small prey like shrimp, but which, in later species became a primary mode of attaining nutrients, using the baleen to filter out krill and other small invertebrates for food. [12]

Head Morphology

General characteristics

Pakicetids had long narrow snouts, which may suggest a specialized feeding method, the diet probably consisting of land animals and freshwater organisms [13]. The eyes were on top of the head, similar to the placement seen in crocodiles. This suggests an amphibious lifestyle [5]. Eyes placed on top of the head allowed the animal to see prey above water while submerged.

Ambulocetids had narrow heads like the pakicetids did [13], although they were slightly larger. The eyes, while still placed dorsally on the skull, had a more lateral position than in pakicetds [5]. In the ambulocetids, structures of the lower jaw that were later associated with sound transmission in more modern groups also appeared [13].

The cranial fossil record for remingtonocetids is quite extensive, and shows that this group was well adapted for swimming, with a long narrow snout. They had widely set eyes which were considerably smaller than those seen in other groups [13]. This suggests that vision was not an important sense for this group. The remingtonocetids had a large middle ear,which indicates that they may have been using hearing for feeding, as modern cetaceans do [5].

Protocetid skulls were characterized by a supraorbital shield, which is a large flat part of the frontal that goes over the front of the eyes, causing them to face laterally rather than forward [13]. Lateral facing eyes were used to observe underwater prey, and are seen in all cetaceans after this point. The trend in eye position becoming more lateral over time indicates the acquisition of aquatic traits. Protocetid eyes were large, unlike those in remingtonocetids [5].

Basilosaurids and dorudontids had short necks, similar to modern cetaceans. Overall head morphology was pretty close to that of modern cetaceans [5].

The cetacean skull is described as having telescoped through evolution, indicated by facial and vault bones flattening and overlapping with each other [14].

Nares

The external nares (nostrils), present in cetaceans as a blowhole, are sealed with valve-like structures called nasal plugs to prevent water from entering the respiratory system. Mysticetes have 2 nares, while odontocetes have 1. The caudal (and dorsal) positioning of the nares allows the animal to breathe at the surface without having to expend energy lifting the head out of the water [14] The change in position of the nares through time is seen in fossil specimens. In pakicetids, the nasal opening was near the front of the snout. The positioning was similar in ambulocetids and remingtonocetids. In protocetids the nasal opening was large and opened over the 4th tooth of the upper jaw, a more caudal position than in previous groups. In the basilosaurids and dorudontids, the nares opened near the 5th tooth. Fossil odontocetes and mysticetes had nasal openings that are more caudal than in basilosaurids, but not as caudal as in modern cetaceans [5].

Tooth morphology

Modern odontocetes have a large number of similar simple, peg-like teeth, a single set over the lifetime. In other words, they’re homodonts and monophyodonts [13]. Mysticetes don’t have teeth, rather a repeated series of baleen plates for food procurement [15]. Eocene cetaceans were heterodonts (had different types of teeth) and diphyodonts (they had 2 sets of teeth over a lifetime). Several authors have argued that diet was a driving force in early cetacean evolution, but it is not known what they ate. Overall, there has been a loss of regional specialization and an increase in the number of repeated elements through dental evolution. Early Eocene odontocetes had more complex teeth, while later forms had less complexity [13]. Since mysticetes don’t have teeth, the transition to homodont dentition may have occurred before the separation of the mysticete and odontocete lineages [16].

Brain size

Cetaceans held the record for the largest relative brain size until humans began to evolve in the late Pliocene [13]. It has been hypothesized that the large brain is due to an aquatic lifestyle. This has been proven not to be true, since the large brain evolved millions of years after the transition to a fully aquatic lifestyle. Many odontocetes possess brains 4 or 5 times larger than would be expected for their body size, represented by a value known as an encephalization quotient (EQ). Mysticetes have much smaller EQs, all falling below 1. This is due to the uncoupling of body and brain size in such large animals, although evidence suggests that mysticete brains have undergone some enlargement over evolutionary history. The large brain size in odontocetes is due to an expanded neocortex, which has a large area associated with higher order integrative functions [17]. The odontocete brain experienced a loss of olfactory structures and the enlargement of auditory structures [5], leading to a large midbrain – this may be due to the acquired use of echolocation. Odontocete brains are so large because they’re socially complex and communicative [17]. They require large brains because they are predators that forage in a 3 dimensional medium [15].

Air sacs

There has been significant change in the respiratory tract structures associated with the head throughout cetacean evolution to accommodate living in water. Modern cetaceans don’t have paranasal sinuses, which are found in terrestrial mammals. This is an adaptation for diving, because since paranasal sinuses are enclosed in bone, they could fracture during ascent or descent in the water due to changing air volume that occurs with changing pressure. Cetaceans have developed air sacs associated with the head. Odontocetes have paranasal sacs which are not completely enclosed in bone and can accommodate air volume changes that occur when diving, therefore eliminating the risk of fracture. They are attached to the airway, but are outside the skull. Mysticetes have a laryngeal air sac. Air sacs may act to increase buoyancy of the head [14].

Development of Echolocation

Ear Morphology: Terrestrial v.s. Marine

The terrestrial mammal ears main features include: the outer ear pinna, external auditory meatus, tympanic membrane, the middle ear ossicles (malleus, incus, and stapes), and the cochlea. A key feature of the land mammal ear is that the tympanic and periotic bones are closely connected and the periotic bone is in close contact with many skull bones, so the ear is not acoustically isolated from the skull, which can result in bone conduction[18]

The modern odontocete ear main features include: a wide mandibular canal known as a mandibular foramen (opens posteriorly on the medial side of the jaw), the mandibular fat pad, the tympanic plate, the middle ear ossicles (malleus, incus, and stapes), and the cochlea. While this is very similar to the land mammal ear there are some key differences. Modern odontocetes do not posses an outer ear pinna and while they do still have the external auditory meatus, it is not functional in hearing.[18] In odontocetes the tympanic membrane is present as an elongated tympanic ligament, instead of the membrane structure formed in land mammals. In land mammal ears the tympanic and periotic bones are closely connected, but in the odontocete ear these connections are greatly reduced and the ear is acoustically isolated through air sinuses that run between the periotic bone and other skull bones.[18] These changes adapted in less than 10 million years and are outlined below. Specialized acoustic fat bodies are also a key component for echolocating. They contain highly organized endogenous lipids with favorable acoustic properties.[19]The mandibular fat pad is one such body while the fat tissue in the melon is another. These fat bodies are composed of branched chain fatty acids, which contribute to the production and reception of echolocation signals.[19]

Pakicetids are thought to be the earliest cetacean transitioning from land to water for they possessed a land mammal ear for hearing in air and used bone conduction underwater. They had a small mandibular foramen in the lower jaw and did not posses a mandibular fat pad.[18] The external auditory meatus was still present at this time and the tympanic membrane closely resembled land mammals.[18]

Ambulocetids evolved slightly compared to the pakicetids for they possessed a mandibular fat pad for use in sound conduction but it is still thought that they had a low sensitivity in hearing due to a thick mandibular wall.[18] Ambulocetids hearing in water was mainly through bone conduction and land hearing was thought to occur by pressing the head to the ground in order to feel the vibrations.

Remingtonocetids had a large mandibular foramen and a thinner lateral mandibular wall than the pakicetids and ambulocetids. Although they had more sophisticated underwater hearing than pakicetids and ambulocetids, presence of the external auditory meatus and other similarities to land mammal ears suggest that remintonocetids were still able to hear in air. The middle ear ossicles closely resembled those of modern odontocete ossicles with minor differences. Due to the similarities between ossicles, it is thought that remingtonocetids had a fully functioning aquatic ear.

Protocetids an external auditory meatus was still present but a wide mandibular foramen and a mandibular fat pad allowed for underwater sound transmission.[18] Unlike remingtonocetids, ambulocetids, and pakicetids, protocetids inner ear morphology allowed for a degree of directional hearing. The ossicular chain was reoriented between remingtonocetids and protocetids, indicating the continuing evolution of the aquatic ear. Protocetids still maintained their land mammal hearing mechanism but had also gained the modern odontocete aquatic hearing mechanism but bone connections between the ear and the skull suggest that protocetids could not echolocate.[18]

Basilosaurids and Dorudontids still possed an external auditory meatus but with a different orientation than protocetids and remingtonocetids. The ossicles are different from those of remingtonocetids and protocetids and the ossicle chain position closely resembled that of the modern odontecete. In basilosaurids and dorudontids air hearing was barely used and aquatic hearing was the main function of the ear, evidenced by reduced skull and ear bone connections.

Types of Echolocation and Uses for Communication

Of the modern cetaceans it is the odontocetes that posses the specialized echolocation systems. Odontocetes are toothed whales and dolphins. In these organisms sound is produced in the nasal system instead of the larynx, and the sound is channeled through the melon, which sits directly in front of the nasal system.[20] Odontocetes echolocate by sending out a click, receive and process the echo, and send out more clicks. These click intervals can be referred to as pulse mode. Odontocetes are able to vary the amplitude of the echolocation signals they produce, known as click-source levels. Odontocetes produce two main signals: whistles and burst pulses. While only some species of odontocetes produce whistles, all produce burst pulses. Echolocation signals are projected in a directional beam,[21] and can be measured using the peak frequency (the frequency of maximum energy), and peak-to-peak source levels (sound pressure 1m from the animal).[21] Odontocetes that are capable of whistling can produce high-level clicks when using high frequencies as well as low amplitude clicks at low frequencies. Non-whistling odontocetes can only produce click signals that are high frequency, low intensity, and narrow bandwidth.[21]

It is believed that echolocation is used for communication as well as for predator avoidance and finding prey. Classifying odontocete sounds and signals is difficult but 6 main categories of whistles have been accepted. These categories are: constant frequency whistles, upsweep whistles, downsweep whistles, concave (hill) whistles, convex (valley) whistles, and sinusoidal (multiple) whistles.[20] Dolphins specifically are capable of developing signature whistles for communication, which are individual specific.[20] Echolocating cetaceans are able to produce pulse chains that function in echolocation, but are also able to produce non-echolocating burst pulse sounds. These sounds are highly directional and there is evidence that both burst pulse sounds and echolocation signals are produced from the same source.[20]

Molecular Genetics

Recent advances of molecular analysis techniques have led to a revision of the phylogenetic position of cetaceans. Previously it was initially thought that cetaceans were a sister group to artiodactyls and were the closest living relative of the extinct mesonychian. In a mitochondrial DNA sequence study including three artiodactyl (cow, pig and sheep), two cetaceans (fin and blue whale), and the newly sequenced mitochondria DNA of the hippopotamus resulted in finding which suggested a monophyletic cetacean and hippopotamus clade.[22] The timing of divergence between cetaceans and hippopotamus is estimated to be about 54 ma BP.[22] In addition to analyzing mitochondrial DNA and protein sequences there has also been new evidence of a cetacean-artiodactyla group by tracing the events of retrotranposon insertion between species. Complete genomic sequencing of cetacean species has allowed for a more in depth comparison of SINEs and LINEs. An initial analysis of short interspersed elements (SINEs) and long interspersed elements (LINEs) or tranposons, resulted in a proposal of a monophyletic group that joined the cetaceans, hippopotamus and ruminants[23]. More recent studies of retrotranposon insertions has supported the idea of a revised phylogeny resulting in a monophyletic cetacean and hippopotamus clade that is found within artiodactyls.[23] At the molecular level, transposons that have been characterized from the whale genome were screened for their presence among the major groups within the cetartiodactyl clade. Distinct SINEs labelled KM14, HIP4, HIP24, and AF from the whale genome loci were observable in both hippopotamus and whale species. The loci HIP5 was found in the ruminants along with the hippopotamus and cetacean group.[23] The evidence provided by retrotranposon analysis results in a monophyletic clade including hippos and cetaceans that is a sister group to ruminants within, and nestled within the artiodactyl order. The retrotranposon analysis of 19 new independent loci within the order cetacean has produced results suggesting the trichotomy classification of toothed whales, baleen whales and dolphins. SINE insertion analysis proposes a monophyletic clade containing sperm whales and dolphins. Nine sequenced retrotranposon are used to support this position. Baleen whales do not share any of those 9 SINE insertions and therefore are consider to be excluded from the monophyletic grouping. The loci characterized from Baleen whales included 10 individual loci that are amplified in a common ancestor of the cetacean clade.[24] The molecular analysis of cetacean evolution has led to a phylogenetic tree supporting the hippopotamus as the closest extant relative to the cetacean clade. It also infers that the suborder Mysticeti diverged first, and the suborder Odontoceti evolved later.


References

  1. ↑ 1.0 1.1 1.2 Thewissen, J. G. M., and L.N. Cooper. From Land to Water: Origin of Whales, Dolphins and Porpoises. Evo. Edu. Outreach. (2009): 272-288. Springer. Web. 10 November 2012.
  2. ↑ Arnason U., Gullberg, A. and Axel Janke. Mitogenomic analyses provide insights into cetacean origin and evolution GENE. (2004): 27-34. Science Direct. Web. 10 November 2012.
  3. ↑ University of California Berkeley. Whale Evolution. Understanding Evolution. Web. 12 Nov. 2012.
  4. ↑ 4.0 4.1 4.2 Prehistoric Whales: The Story of Whale Evolution. About.com Guide. Web. 10 Nov. 2012.
  5. ↑ 5.0 5.1 5.2 5.3 5.4 5.5 5.6 5.7 Thewissen, J. G. M., and Sunil Bajpai. “Whale Origins as a Poster Child for Macroevolution.” Bioscience 51.12 (2001): 1037-1049. BioOne. Web. 30 October 2012.
  6. ↑ Introduction to Cetacea. University of California Museum of Paleontology. Web. 10 Nov. 2012.
  7. ↑ Geisler, Jonathan H., and Mark D. Uhen. ‘Morphological Support for a Close Relationship Between Hippos and Whales’. Journal of Vertebrate Paleontology 23.4 (2003): 991–996. Web. 21 Nov. 2012.
  8. ↑ 8.0 8.1 8.2 8.3 8.4 8.5 Bejder, Lars, and Brian K. Hall. ‘Limbs in Whales and Limblessness in Other Vertebrates: Mechanisms of Evolutionary and Developmental Transformation and Loss’. Evolution & Development 4.6 (2002): 445–458. Web. 21 Nov. 2012.
  9. ↑ Arif, M., S.T. Hussain, and J.G.M. Thewissen. "Fossil evidence for the origin of aquatic locomotion in archaeocete whales." Science 263.5144 (1994): 210+. Health Reference Center Academic. Web. 21 Nov. 2012.
  10. ↑ Buchholtz, Emily A. ‘Modular Evolution of the Cetacean Vertebral Column’. Evolution & Development 9.3 (2007): 278–289. Web. 21 Nov. 2012.
  11. ↑ Meyer, Wilfried, Klaus Neurand, and Milan Klima. ‘Prenatal Development of the Integument in Delphinidae (Cetacea: Odontoceti)’. Journal of Morphology 223.3 (1995): 269–287. Web. 21 Nov. 2012.
  12. ↑ Fitzgerald, Erich M. G. ‘A Bizarre New Toothed Mysticete (Cetacea) from Australia and the Early Evolution of Baleen Whales’. Proceedings of the Royal Society B: Biological Sciences 273.1604 (2006): 2955–2963. Web. 21 Nov. 2012.
  13. ↑ 13.0 13.1 13.2 13.3 13.4 13.5 13.6 13.7 Thewissen, J. G. M., and E. M. Williams. “The Early Radiations of Cetacea (Mammalia): Evolutionary Pattern and Developmental Correlations.” Annu. Rev. Ecol. Syst. 33 (2002): 73-90. JStor. Web. 29 October 2012.
  14. ↑ 14.0 14.1 14.2 Reidenberg, Joy S., and Jeffrey T. Laitman. “Sisters of the Sinuses: Cetacean Air Sacs.” The Anatomical Record 291 (2008): 1389-1396. Wiley InterScience. Web. 1 November 2012.
  15. ↑ 15.0 15.1 Wursig, Bernd. “Cetaceans.” Science 244 (1989): 1550-1557. JStor. Web. 23 October 2012.
  16. ↑ Macleod, C. D., J. S. Reidenberg, M. Weller, M. B. Santos, J. Herman, J. Goold, and G. J. Pierce. “Breaking Symmetry: The Marine Environment, Prey Size, and the Evolution of Asymmetry in Cetacean Skulls.” The Anatomical Record 290 (2007): 539-545. Wiley InterScience. Web. 30 October 2012.
  17. ↑ 17.0 17.1 Marino, Lori. “Cetacean Brains: How Aquatic Are They?” The Anatomical Record 290 (2007): 694-700. Wiley InterScience. Web. 29 October 2012.
  18. ↑ 18.0 18.1 18.2 18.3 18.4 18.5 18.6 18.7 Nummela, S. Thewissen, J.G.M. Bajpai, S. Hussain, T. Kumar, K. “Sound Transmission in Archaic and Modern Whales: Anatomical Adaptations for Underwater Hearing.” The Anatomical Record 290 (2007): 716-733. Wiley InterScience. Web. 16 Nov. 2012.
  19. ↑ 19.0 19.1 Koopman, H.N. Zahorodny, Z.P. “Life History Constrains Biochemical Development in the Highly Specialized Odontocete Echolocation System.” Proceedings of the Royal Society B. 275 (2008): 2327-2334. The Royal Society. Web. 17 Nov. 2012.
  20. ↑ 20.0 20.1 20.2 20.3 Au, W.W.L. Hastings, M.C. “Emission of Social Sounds by Marine Animals.” Principles of Marine Bioacoustics. Springer Science and Business Media. 2011. 401-490. Web. 17 Nov. 2012.
  21. ↑ 21.0 21.1 21.2 Au, W.W.L. Hastings, M.C. “Echolocation in Marine Mammals.” Principles of Marine Bioacoustics. Springer Science and Business Media. 2011. 501-559. Web. 17 Nov. 2012.
  22. ↑ 22.0 22.1 Ursing,B.M.; U. Arnason . "Analyses of mitochondrial genomes strongly support a hippopotamus-whale clade". 1998 Proceedings of the Royal Society 265 (1412): 2251–5. doi:10.1098/rspb.1998.0567
  23. ↑ 23.0 23.1 23.2 Nikaido, Masato. Rooney, Alejandro. Okada, Norihiro. “phylogenetic relationships among cetartiodactyls based on short and long interspresed elements: Hippopotamuses are the closet extant relative of whales.” 1999 PNAS 96 10261-10266 doi:10.1073/pnas.96.18.10261
  24. ↑ Nikaido, M., F. Matsuno, H. Hamilton, R. L. Brownell Jr., Y. Cao, W. Ding, Z. Zuoyan, A. M. Shedlock, R. E. Fordyce, M. Hasagawa, and N. Okada. Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. 2001. Proc. Natl. Acad. Sci. USA 98:7384–7389.
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