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Cetacea

Whales, dolphins, and porpoises

Michel C. Milinkovitch and Olivier Lambert
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A striped dolphin surfacing in the Mediterranean Sea between France and Corsica.
taxon links [up-->]Mysticeti [up-->]Odontoceti extinct icon Not MonophyleticMonophyly Uncertain[down<--]Eutheria Interpreting the tree
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Archaeoceti clearly is paraphyletic, Mysticeti clearly is monophyletic, Odontoceti is likely monophyletic (see text below).
Containing group: Eutheria

Introduction

Cetaceans (whales, dolphins and porpoises) form one of the most dramatically-derived group of mammals. Indeed, during their transition from the terrestrial to the aquatic environment, they experienced spectacular transformation of many biological systems and acquired a fusiform body shape giving modern families a superficial resemblance to fish. Extant cetaceans comprise approximately 87 species in 14 families and two sub-orders: Mysticeti (baleen-bearing whales) and Odontoceti (teeth-bearing whales) (Rice, 1998). Adult size ranges from less than 1.5 meters for some representatives of the Cephalorhynchus genus, to more than 30 meters for the largest blue whales. Cetaceans are ecologically very diverse as their habitats vary from coastal to pelagic, from tropical to polar, and from marine to fresh water, while their preys vary from planctonic crustaceans to fish, squids, and marine mammals.

Characteristics

The major morphological transformations related to the transition to the aquatic environment include:

Breathing

In mysticetes the nasal passages are separate tubes all the way to the external nares, whereas in odontocetes, the two nasal passages branch into a complex series of nasal sacs that eventually coalesce into a single blowhole. The sperm whale is however intermediate as it exhibits a sigmoidally-shaped blowhole formed by two nasal tubes that remain distinct from the bony nares to the top of the head: the anterior and posterior curves of the sigmoid blowhole represent the apertures of the right and left nares, respectively (rare examples of adult sperm whales with two distinct blowholes have even been reported). In the pygmy sperm whales (Kogiidae), the situation is only slightly different since the nasal passages remain discrete tubes until just proximal to the single blowhole.

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Toothed whales have a single blowholeBaleen whales have two blowholes.

Left: Toothed whales have a single blowhole. Right: Baleen whales have two blowholes. © Michel C. Milinkovitch

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In the giant sperm whale, the nasal passages remain discrete tubes until just proximal to the single s-shaped blowhole.

In the giant sperm whale, the nasal passages remain discrete tubes until just proximal to the single s-shaped blowhole.
© 1989 John E. Heyning.

 

Hearing and Echolocation

Echolocation is the ability to assess the environment (mostly, detecting obstacles, conspecifics, predators, and prey) by emitting sounds and listening to the echoes. Echolocation abilities have been conclusively demonstrated in delphinoids and so-called “river dolphins” (see below) and seem to be present in beaked and sperm whales as well. Although they can easily detect an object about the size of a ping-pong ball more than 50 meters away, dolphins also use echolocation to inspect objects at very short ranges (e.g., to assess shape, size, and structure). Dolphins produce short “clicks” whose frequencies (10 to 150 kHz) and intervals (as short as 1.2 milliseconds) are adjusted depending on the size and distance of the target (high frequencies dissipate more rapidly than low frequencies but allow the detection of smaller targets and a finer analysis of shape and structure). These sounds are produced by circulation of air in a complex system of facial sacs, reflected by the cranium, and focused into a beam by the melon, a fatty structure located in the forehead and serving as an acoustic lens. Mysticetes possess a small (Heyning 1989), possibly vestigial (Milinkovitch, 1995) melon.

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The melon is a a fatty structure located in the forehead of all cetaceans. In most toothed whales, it serves as an acoustic lens for echolocation sound production. The melon is shown in blue for the genera Globicephala, Inia, Ziphius, Balaena, and Physeter (from left to right). S, spermaceti organ.
© 1995 Michel C. Milinkovitch

The high-frequency echoes are received through the hollow mandible then transferred across fatty channels to the middle ear. Low-frequency sounds on the other hand are perceived through the auditory channels. The middle and inner ears of odontocetes are surrounded by an emulsion of mucus, oil, and air. The whole structure is enclosed into a dense, bony bulla. This high level of acoustic isolation greatly improves directional detection. The isolation mechanism is less complete in mysticetes, but the large distance between the two ears (simply because of the size of these animals) probably helps directional detection. Mysticetes exhibit a peculiar tympanic membrane (the finger glove) and seem to receive sounds through the auditory channels. It is unclear whether mysticetes are able to rely on the echoes of their low-frequency sounds.

Dorsal and anterior to the skull, sperm whales also have a large oily organ (called the “spermaceti organ” because early whalers thought the whitish oily substance was the whale semen) that possibly works as a biological ballast (Raven & Gregory 1933; Clarke 1970) or constitutes a secondary sexual character involved in acoustic display (Cranford 1999). Because of the high specialization of the giant sperm whale facial anatomy, it is unclear what structure in this species is homologous to the melon of other cetaceans. However, based on the comparison between the facial anatomy of dwarf and pygmy sperm whales, Heyning (1989) suggested the junk (a segmented tissue located below the spermaceti case and so-called because it is less rich in oil than the spermaceti itself) rather than the spermaceti organ as the most likely candidate. This hypothesis is supported by comparative CT-scan analyses (Cranford et al. 1996).

Origin of Cetacea

The oldest known cetaceans are Eocene in age, appearing around 55 million years ago. These primitive toothed cetaceans, lacking odontocetes and mysticetes cranial specializations, form the paraphyletic sub-order Archaeoceti. Representatives of this group have been found in Egypt, Nigeria, India, Pakistan, and USA and show a wide range of morphologies that prompted their classification into several families such as the Pakicetidae (early Eocene), Protocetidae (middle Eocene) and Basilosauridae (middle to Late Eocene). The most primitive taxa exhibited locomotory hind limbs (see Thewissen et al. 1994; Gingerich et al. 2001; Thewissen et al. 2001). The archaeoceti fossils illustrate the progressive reduction of hind limbs, adaptations of the ear for underwater hearing, and the expansion of the pterygoid sinus fossae in the basicranium leading to a better isolation of the ear bones.

 

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Skeleton of Rhodocetus kasrani. Forelimbs were probably folded against the body during rapid swimming by pelvic paddling at the sea surface and during rapid swimming by pelvic paddling and caudal undulation when submerged. On land, Rodhocetus supported itself on hoofed digits II, III, and IV of the hands and on the plantar surfaces of the feet, and probably progressed somewhat like a modern eared seal or sea lion. Drawing from Gingerich et al. 2001. © 2001 American Association for the Advancement of Science

The origin of aquatic cetaceans has to be found among terrestrial mammals living in the early Tertiary. Analyses of neontological data have long suggested that cetaceans are closely related to ungulates (e.g., Flower, 1883; Prothero et al. 1988). These results were corroborated by paleontological data (Gingerich et al. 1990; Thewissen and Hussain, 1993; Thewissen, 1994). The close relationship between cetaceans and ungulates (and especially artiodactyls) was strongly supported by basically all molecular data published to date: from immunological (e.g., Boyden and Gemeroy, 1950; Shoshani, 1986) and DNA-DNA hybridization (Milinkovitch, 1992) studies, to analyses of mitochondrial and nuclear amino-acid and DNA sequences (e.g., Czelusniak et al. 1990; Milinkovitch et al. 1993; Gatesy, 1997; Milinkovitch et al. 1998, Gatesy et al. 1999).

The two main alternative hypotheses regarding the exact phylogenetic position of cetaceans within mammals are suggested respectively by morphological and molecular data. Morphological studies suggested that artiodactyls is the sister group to Cete -- i.e., a clade comprising cetaceans and a fossil group of carnivorous hoofed mammals: the mesonychians (see e.g. O'Leary and Geisler, 1999). On the other hand, molecular studies indicate that cetaceans are highly derived artiodactyls and that hippopotamids are their extant sister group. Although the nesting of cetaceans within artiodactyls (making the latter paraphyletic) was suggested by multiple studies (Goodman et al. 1985; Czelusniak et al. 1990; Irwin et al. 1991; Graur and Higgins, 1994; Gatesy et al. 1996; Smith et al. 1996; Gatesy, 1997; Montgelard et al. 1997) the statistical support or methods of analyses have been strongly criticized (e.g., Philippe and Douzery, 1994; Hasegawa and Adachi, 1996). This lead to a second series of molecular analyses with greatly increased taxon and gene sampling (Milinkovitch et al. 1998, Gatesy et al. 1999).

These latter analyses confirmed the monophyly of Cetartiodactyla (cetaceans,artiodactyls) and clarified its phylogeny. Furthermore, phylogenetic interpretation of retropositional events that lead to the insertion of short interspersed elements (SINEs) at particular loci in the nuclear genome of various artiodactyl and cetacean ancestors (Shimamura et al. 1997; Nikaido et al. 1999) lead to the same phylogenetic tree, suggesting that the paraphyly of artiodactyls is not the result of analytical problems related to the analysis of aligned nucleotide sequences (Milinkovitch and Thewissen, 1997; Shedlock et al. 2000). It is indeed the nature of SINE data that makes them so efficient in phylogeny inference: the likelihood of SINEs being independently inserted at the same locus in different lineages, or precisely excised in different lineages, seems virtually nil.

It remains to be understood why these results are in striking contradiction to the common interpretation of the available morphological data, namely, supporting artiodactyl monophyly (e.g., O'Leary and Geisler, 1999).

Note however, that the discrepancies between the morphological and molecular hypotheses have recently diminished. Indeed, recent discoveries of primitive whales from the families Pakicetidae and Protocetidae, from the early Eocene of Pakistan, allowed the description of skulls associated with hindlimbs (Thewissen et al. 2001; Gingerich et al. 2001). These fossils exhibit skull characters typical of primitive cetaceans and terrestrial hindlimbs with derived characters of artiodactyls. The morphology of the ankle (mainly the astragalus and calcaneum) of these terrestrial cetaceans suggest that Cetacea are the sister group of monophyletic Artiodactyla, and that [artiodactyls , cetaceans] form the sister group of mesonychians. In these new trees, cetaceans are therefore getting closer to artiodactyls but these analyses of morphological characters continue to support the monophyly of the latter group and, hence, to disagree with the molecular analyses.

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Relationships between Artiodactyla, Cetacea, and Mesonychia based on morphological data.

Relationships between Artiodactyla, Cetacea, and Mesonychia based on morphological data. From Thewissen et al. (2001).

Finally, Geisler and Uhen (2003) have performed maximum parsimony analyses of a matrix including substantially more taxa and morphological characters than previous analyses and found support for the sister-relationship between hippos and cetaceans, making molecular and morphological evidence for the phylogeny of these taxa much more congruent than previously thought.

Discussion of Phylogenetic Relationships

Some molecular studies based on mitochondrial DNA sequences (Milinkovitch et al. 1993; Milinkovitch et al. 1994) suggested that Physeteroidea (sperm whales) are more closely related to mysticetes than they are to other odontocetes. However, other molecular data (e.g., Nikaido et al. 2001; Gatesy et al. 1999) support the monophyly of toothed whales (Odontoceti). Recent analyses (Cassens et al. 2000) indicate that there is conflicting signal between the nuclear DNA and mitochondrial DNA data. Whether this conflict is due to differential lineage sorting or to misleading signal from one or several data set(s) remains to be investigated. This issue is further discussed in the Odontoceti (toothed whale) page.

Phylogenetic relationships among the families of extant cetaceans are still problematic and hypotheses on various nodes of the tree come from a variety of data: the morphology of extant taxa (including the soft anatomy) (e.g., Heyning, 1989), paleontological (e.g., Muizon 1991; Fordyce 1994; Geisler and Sanders 2003), and molecular evidence (e.g., Milinkovitch et al. 1993, 1994; Arnason and Gulberg, 1996; Cassens et al. 2000) or a combination of these (Milinkovitch 1995; Messenger and Mc Guire, 1998; Gatesy et al. 1999). This evidence will be discussed on relevant pages of cetacean subgroups.

Other Names for Cetacea

References

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Gatesy, J., Milinkovitch, M. C., Waddell, V. and Stanhope, M. 1999. Stability of Cladistic Relationships between Cetacea and Higher Level Artiodactyl Taxa. Systematic Biology 48:6-20.

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Information on the Internet

Early Cetacea Fossils:

Title Illustrations
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A striped dolphin surfacing in the Mediterranean Sea between France and Corsica.
Scientific Name Stenella coeruleoalba
Location Mediterranean Sea, between France and Corsica.
Copyright © 1991 Michel C. Milinkovitch
About This Page

Michel C. Milinkovitch
Genetics & Evolution, University of Geneva

Olivier Lambert
Royal Institute of Natural Sciences (Belgium)

Correspondence regarding this page should be directed to Michel C. Milinkovitch at

All Rights Reserved.

Citing this page:

Milinkovitch, Michel C. and Olivier Lambert. 2006. Cetacea. Whales, dolphins, and porpoises. Version 07 August 2006 (under construction). http://tolweb.org/Cetacea/15977/2006.08.07 in The Tree of Life Web Project, http://tolweb.org/

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