Cetaceans: A Case Study in Macroevolution by Sean Chamberlin
The study of evolution—the change in species over time—involves many aspects beyond the scope of my treatment here. However, the cetaceans offer an ideal example in the study of how the vertebrate body plan was modified from a terrestrial form to an aquatic one. Rapid advances in our knowledge of cetaceans, spurred in part by new fossil finds in Pakistan, India and elsewhere, have provided scientists with “one of the best documented examples of macroevolution in mammals” (Thewissen and Bajpai 2001).
Macroevolution, the evolution of higher-order taxa above the species level, helps to explain trends in evolution that occurred as a result of changes in the global environment, brought about by shifts in climate (with tectonic, biological or astronomical causes, among others), catastrophic events (such as mass eruptions or meteorite impacts) or other causes. Microevolution, the evolution of new species, represents an important part of macroevolutionary processes and modern ecological theory encompasses both (see Mayr 2001; Gould 2002). The global scale events that drive macroevolution may eliminate entire groups of species (higher-order taxa) and provide new habitat that may be exploited by surviving species, i.e., new ecological opportunity (Schluter 2000). The success with which an organism exploits this new environment and diversifies into many species is called adaptive radiation. More formally adaptive radiation may be defined as “the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage.” Fundamentally, it explains how a single ancestor diversifies into a number of species in a diverse environment. For instructors and inquiring minds interested in learning more on these topics, we suggest Ernst Mayr’s What Evolution Is (2001) or the National Science Teacher Association publication Evolution in Perspective (2003).
The exploitation of a shallow marine habitat by a land mammal and its transition to a fully aquatic animal that rapidly diversified throughout the world ocean in response to shifts in climate describes the macroevolution of cetaceans. A brief discussion of this evolutionary history provides insights into how small changes in the body plan of an organism—often brought about by small changes to a single gene or set of genes—can lead to different functions and enable an organism to exploit otherwise unavailable resources. Cetaceans are highly modified mammals but they are mammals nonetheless. The fossil record and a host of other evidence now offer a fairly complete picture of their transition.
Until 2001, scientists held two hypotheses regarding the ancestry of cetaceans. Palaeontological evidence suggested that they came from a wolf-like, mesonychian ancestor, a relative of hooved ungulates like the cow. DNA data supported an origin from an ariodactyl ancestor, an even-toed ungulate like the deer or hippopotamus. Combining morphological, protein and DNA data and adding results from studies of newly discovered cetacean skeletons called pakicetids, scientists now agree that ariodactyls are the base ancestor. However, their relatedness to hippopotamids is not direct. Thewissen suggest that cetaceans and hippos may have shared the same “grandmother” but additional research will be needed to establish these relationships unequivocally (e.g. Thewissen et al., 1998, 2001). Establishing phylogenetic relationships within the Cetacea will also require additional studies. (Berta and Sumich 1999; see also Gatsey et al., 1996).
Nevertheless, modern fossil and molecular evidence allow us to trace the stages in the evolution of early cetaceans, perhaps better than any other animal (Thewissen and Bajpai 2001). The very first fossil cetaceans, called archaeocetes (“ancient whales”) or, on occasion, “experimental Eocene whales” (Thewissen and Williams 2002), appear about 50 million years ago in Pakistan and India, where cetaceans are thought to have evolved in the Tethys seaway. The “experimental” qualifier of these animals stems from the observation that a variety of morphological characteristics typified these animals, serving to provide diverse modes of feeding and behavior in a relatively stable habitat. However, as their habitat was transformed by tectonic, atmospheric and other global processes, most of these experiments went extinct. As Thewissen (1998) puts it: “Cetaceans originated when a Paleogene land mammal underwent a dramatic shift in biological attributes in order to accommodate an enormous shift in habitat.”
These first cetaceans were not aquatic; rather, they walked on all fours and merely spent a great deal of time wading in water. With time, evolution (for reasons speculated below) continued to favor animals adapted for an aquatic life and the cetaceans developed a more “whale-like” posture. The ambulocetidae, a group of early cetaceans—similar to the crocodiles in their habit of waiting in water and ambushing prey on shore—flourished in the Eocene about 49 million years ago. By the late Eocene, approximately 35 to 41 million years ago, the advanced archaeocetes, the basilosaurids and dorudontids, whose fossils are abundant in the eastern United States, had invaded the ocean. With a toothed upper and lower jaw, a horizontally flattened tail and nostrils on top of its head, these whales most closely resemble the modern whales. Though they went extinct at the start of the Oligocene, 34 million years ago, they left behind two very important descendants: the Odontocetes and the Mysticetes.
Cetaceans quickly radiated (diversified into different species) throughout the world ocean about 28–33 million years ago. What is perhaps most remarkable about this feat is how the cetacean body transformed from a terrestrial existence to an aquatic one. Scientists consider cetaceans to be the most highly derived (exhibiting the greatest number of changes) among all mammals. Their skull telescoped—elongated in the anterior-posterior and lateral directions—to accommodate their dorsally migrating nostrils that eventually became their blowhole, the opening through which they breathe. Breathing through the top of their head, as it were, enabled cetaceans to spend less time at the surface, perhaps to avoid predators, and to conserve energy by reducing drag associated with surface swimming. Elongation of the skull and shortening of the neck streamlined their body, further enhancing their hydrodynamic abilities. Evolution of a horizontally flattened tail, called a fluke, provided a highly efficient hydrofoil for propulsion. Loss of the hindlimbs and modification of the forelimbs into flippers for steering completed the morphological transformation to a wholly aquatic life.
The transition to the ocean also required modification of the cetacean sensory system. The limited visual and olfactory environment of the ocean—relative to terrestrial environments—led to complex modifications of the lower jaw and inner ear to accommodate underwater hearing. Sound travels underwater about 4.5 times the speed of sound in air, attenuates much less rapidly than light and travels far more quickly than chemical cues, so hearing has increased greater importance in the ocean. At the same time, limitations imposed by swimming in three dimensions, diving (and equilibrium of the ear) and reliance on echolocation, communication and mating led to additional specializations, many of which are still poorly known. As emphasized on the Paleos web site, the “ear” functions for more than just sensing sound; it also functions in balance and detecting acceleration. These simultaneous demands on the auditory system of cetaceans complicate their evolution and make them more difficult to study. Nonetheless, the study of cetacean hearing has gained prominence in the 21st century. The proposal to use acoustics for measuring rates of ocean warming (acoustic thermometry) and the Navy’s desire to use low-frequency active sonar (LFAS) have prompted outcries over their potential negative effects on cetaceans, including disruption of their hearing. Thus, our study of cetacean hearing takes on added dimensions for interpreting this modern debate.
The ear flaps, or pinnae, of cetaceans are absent, presumably to reduce drag. Ear canals may be present in some species and these are nearly always filled. The air-filled canal between the ear and ear drum—like that found in humans and most other mammals—is absent in cetaceans. Moreover, their ear drum and inner ear bones, while resembling other mammals, are enclosed in a discrete and specialized “foam-filled” bony space separate from the skull, called a tympanoperiotic complex. The ear drum is not a thin membrane but instead consists of a cord-like structure called a tympanic (or tympanoperiotic) bone connected by ossicles (bony structures) to the inner ear. The inner ear contains all the elements common to the human inner ear, including the semicircular canals, which are much more compact and reduced in size relative to the size of the animal. In fact, the semicircular canal of the blue whale—an animal that reaches lengths of 100 feet—is about the same size as the human semicircular canal (Stokstad 2003). Scientists hypothesize that the “shrinking” of the semicircular canal in cetaceans allows them to perform highly acrobatic maneuvers underwater without losing their balance. In humans, the equivalent movements make us dizzy and/or sick. The lower jaw of cetaceans—at least the toothed ones—also functions in hearing by acting as a conduit or channel for ultrasonic, high frequency sounds used in echolocation (e.g. Aroyan 2001). The use of the lower jaw in sound reception, called mandibular hearing, is not unique to cetaceans but may be used by other vertebrates as well.
A number of physiological adaptations also accompanied the evolution of cetaceans into the ocean, including salt-and-water balance or osmoregulation. Osmoregulation concerns the proper maintenance of salts and water in the body and involves a number of processes, including loss of water through breathing, sweating, urination, defecation, crying (lacrimation) or lactation and gaining of water and salts through drinking or eating. In cetaceans, it appears that the primary means by which they maintain water balance is through diet and metabolic production of water in digestion (Ortiz 2001) but by no means are studies conclusive or comprehensive for all cetaceans. Physiological measurements on large animals who live underwater are understandably difficult. Although scientists are uncertain how cetaceans osmoregulate, they can from the fossil record determine at what stage in their evolution osmoregulation became important. Because freshwater and saltwater differ in their oxygen isotope ratios, scientists hypothesized that the bones of fossil cetaceans may hold clues regarding the source of water ingested by these animals. An analysis of the oxygen isotope ratios of the teeth of several cetacean fossils revealed the timing and transition of these animals to a marine environment in the middle Eocene (e.g. Roe et al., 1998). The application of stable isotopes to understanding the physiology of ancient marine organisms provides an additional tool for understanding the evolution of these animals, their diets and the climate in which they lived (e.g. Kohn 1996).
Thermoregulation in cetaceans involves a rete mirabilia system similar to that we discussed for tuna and other scromboid fishes. These countercurrent heat exchangers (CCHE) conserve heat with a network of thin-walled veins surrounding arteries such that cooler venus blood from the animal’s periphery is warmed by the arterial blood. The CCHE also function to cool the temperature-sensitive reproductive organs of the animals which have evolved to their internal position presumably in response to selective pressure for streamlining. The male testes of cetaceans—wedged between the locomotor muscles of the animal where may they experience overheating—require cooling to prevent overheating and maintain sperm production. The CCHE becomes particularly important for animals who remain submerged for long periods of time, like the sperm whale. The CCHE of sperm whales is one of the most highly developed of all cetaceans with rete mirabilia around the brain, spinal cord and nervous systems, as well as the spermaceti organ, which is thought to function in echolocation (Melnikov 1997).
A provocative hypothesis concerning the evolution of the CCHE in testicular cooling poses that this feature represents an arrested embryonic state, i.e. during development the testicles are prevented from descending in the manner typical of most mammals. The retention of embryonic or juvenile characteristics in adults is known as paedomorphosis, a type of development that may explain the evolution of certain adaptations in organisms (e.g. Pabst et al., 1998). Studies of gene regulatory processes in the embryogenesis and development promise to advance considerably our understanding of the mechanisms leading to adaptive radiation and evolution (e.g. Thewissen and Williams 2002). Identification of the genes responsible for the loss of pelvic fins in sticklebacks—a marine goby-like fish—provide one example (Shapiro et al. 2004).
Of course, cetaceans also maintain a high degree of insulating blubber whose lipid composition varies within and among species. These differences in blubber types led to preferential selection of some species over others by whalers. The lipid content of blubber determines the thermal conductivity of the animal: more heat is retained when the lipid concentration is higher. Thus, tropical species tend to have thinner blubber with a lower lipid concentration than temperate and cold-water species. Dolphins (and probably other cetaceans) may gain or lose blubber in response to colder or warmer conditions (see Berta and Sumich 1999 for further discussion).
Transformation of a land-based mammal to an aquatic one also demanded greater brain-power. The cetacean brain is second only to humans in degree of encephalization—a measure of the size of the brain versus the weight of the animal. Cetacean brains exhibit considerable differences from other mammals, including reduction of the olfactory and limbic lobes, as might be expected and enlargement of brain regions involved in auditory functions and enlargement and elaboration of the neocortex, involved in cognitive and behavioral activities. Given the diverse and advanced behaviors of dolphins, it may not be surprising that they exhibit highly developed brains. However, it is not as apparent what caused the development of such highly a highly sophisticated brain. To answer that, we must look at the environment in which cetaceans evolved and speculate on the selective pressures that may have shaped their evolution.
Note 1: Many aspects of evolution remain controversial, even among scientists, yet the occurrence of evolution on our planet is indisputable, at least among rational-minded people. An excellent overview of evolution and the evidence that supports it can be found at the Talk Origins web site, http://www.talkorigins.org/. See especially their FAQ.
Note 2: Many textbooks, web sites, and documentaries continue to promote the “wolf-ancestor” theory for the evolution of whales, an idea that appears rejected. However, as additional cetacean fossils are found and more complete genomic sequences are compared, the phylogenetic relationships among cetaceans may change. It is always advisable to check your sources and draw conclusions based on multiple authors, present company included.
Note 3: An excellent overview of the evolution of the jaw in vertebrates and its relationship to the development of the inner ear of mammals can be found in Gould’s Dinosaur in a Haystack (1995).