[Note: This post isn’t quite as comprehensive as I would have liked, and I want to add some more illustrations from my other computer, so don’t be surprised if it changes a bit over the weekend. Still, I hope you enjoy it!]
When I was in the 4th grade, I took one of my first trips to the National Aquarium in Baltimore, MD, and I was absolutely in awe of the building and the creatures it contained. Although I can’t remember much from that early visit, I do recall one particular exhibit on the 2nd floor just above the food court. Sunk into a wall was a glass case, and in that glass case was a replica of half of the body of a Beluga whale, form the tip of the tail to about halfway up the back. Sticking out of that case was a lever, and when pushed up or down the whale’s tail moved up or down in the water in the display; I was definitely impressed by the amount of power it took to get the tail to move at even a constant, slow rate of speed. Unfortunately the display isn’t there anymore, but it did spark my imagination about how evolution could have made an animal that swam moving its spine up and down rather than side-to-side like a shark. How could dolphins and sharks be so similar, but so different in the way they moved?
One of the most celebrated evolutionary narratives is that of the first fish/tetrapod (“fishapod”) crawling out of the “primordial ooze” onto dry land. Even though we are only distantly related to such creatures through common ancestry, the move from the water to a more terrestrial habitat is regarded as one of the greatest evolutionary innovations ever to occur, paving the way for all the great tetrapods of subsequent ages. In popular culture, this is where many satirical (and sometimes serious) “March of Progress” like diagrams start, usually featuring some goofy-looking fish with legs on, monkeys seemingly having evolved from such creatures in the blink of an eye (thus allowing humans, in turn, to evolve). This view, of course, doesn’t do any justice to the larger evolutionary truth of the situations, and if we are to understand why dolphins and whales swim the way they do we need to at least start with the evolution of early amphibious vertebrates.
Although the living coelacanth Latimeria chalumnae did not give rise to the first tetrapods (it’s closest fossil relative seems to be the coelacanth Macropoma from the late Cretaceous of England and Czechoslovakia), it is a sarcopterygiian fish and so it can give us some clues as to what adaptations these “lobe-finned” fish had that allowed them to evolve and colonize more terrestrial habitats. Outside of having the proper bone structure that would provide antecedents for the limbs of later tetrapods, sarcopterygiian fish can move their pectoral and pelvic fins independently of each other, almost in a walking type of motion in the water. This video, shot recently in Indonesia, shows this type of motion (although the fish in the video is trying to stay in one place more than swim away);
This type of locomotion, based upon the movement of the fins/limbs rather than the spine/tail, proved to the be precursor of early tetrapod movement. With the limbs carried out to the sides rather than under the body, the head would have to be swung back and forth in the same manner that many fish swam, the position of the arms and legs making it impossible to do otherwise. This sort of side-to-side S-shape movement can still be seen today in living amphibians like salamanders;
The next big advancement that we are concerned with is the transition from carrying the arms on the side of the body to carrying them underneath the body, allowing organisms that were adapted in this manner to be much more active. This change was originally said to have been the main reason why dinosaurs succeeded when so many other creatures of the early Triassic did not, although recent finds like Effigia have shown that dinosaurs were not alone in developing a bipedal stance. The group that we’re primarily concerned with here, however, is not archosaurs but mammals and their close relatives. While many synapsids like Dimetrodon still had a sprawling stance inherited from its amniote ancestors, by the Cretaceous mammals were carrying their legs directly underneath their bodies, or at least very nearly so (thanks for the correction johannes). This change allowed the animals to move away from a side-to-side wrenching of the vertebral column on the horizontal axis and allow the spine to undulate on the vertical axis, allowing for faster and more efficient movement. The success of this kind of movement can perhaps best be exemplified today by the fastest terrestrial mammal on the planet, the cheetah;
Going back to the Triassic, however, mammals were still evolving and skittering about while dinosaurs, plesiosaurs, icthyosaurs, pterosaurs, and the other superstars of the Mesozoic were undergoing their own evolution. The archosaurs that returned to the water seemed to undertake at least two strategies, plesiosaurs primarily using their flippers for propulsion like modern-day sea turtles while icthyosaurs started off with more snaky, catshark-like motions, the most derived forms becoming evolutionarily convergent with lamnid sharks (like the Shortfin Mako) and tuna. Mosasaurs, which arrived late on the scene, seemed to employ something of a mix of the two strategies, using long bodies with powerful tails and flippers for propulsion. The earliest-known relatives of living whales, however, would not be progressing on their own aquatic evolution until about 13 million years after the last dinosaurs died out at the K/T boundary, the great marine reptiles being long gone by the time of Pakicetus during the Eocene.
Outdated reconstruction of Pakicetus, and how I was first introduced to the creature in a children’s book.
Modern reconstruction of Pakicetus
[Illustration by Carl Buell, and taken from http://www.neoucom.edu/Depts/Anat/Pakicetid.html]
The problem with the evolution of whales was that their fossil history was largely a mystery until relatively recently. Charles Darwin, in the first edition of his landmark On the Origin of Species by Natural Selection, hypothesized that carnivorous mammals could be adapted to an aquatic lifestyle given enough time. In Chapter 6, Darwin wrote;
In North America the black bear was seen by Hearne swimming for hours with widely open mouth, thus catching, like a whale, insects in the water. Even in so extreme a case as this, if the supply of insects were constant, and if better adapted competitors did not already exist in the country, I can see no difficulty in a race of bears being rendered, by natural selection, more and more aquatic in their structure and habits, with larger and larger mouths, till a creature was produced as monstrous as a whale.
This passage, although there is no real fault in it, gave Darwin plenty of grief as many thought he was suggesting that black bears had evolved into whales. It is easy to tell from the passage, however, that this is not the case, and a letter to Charles Lyell dated December 10, 1859 further shows that Darwin was not trying to prove such a narrow point. Referring to an interview with the “bitter & sneering” Richard Owen about his book, Darwin writes;
Lastly I thanked him for Bear & Whale criticism, & said I had struck it out. — “Oh have you, well I was more struck with this than any other passage; you little know of the remarkable & essential relationship between bears & whales”. —
I am to send him the reference, & by Jove I believe he thinks a sort of Bear was the grandpapa of Whales!
Indeed, the reaction to this passage was certainly overblown (Darwin may yet be vindicated to some extent as some variety of bear seem to be a fair candidate for the ancestor of pinnipeds) and even after the criticism Darwin still maintained that the process of changing a bear into a more aquatic animal is possible. Still, a suitable ancestor for whales was elusive, even the great Basilosaurus offering no definite answers. Discovered in the early 1800’s, fossils of the whale Basilosaurus (=”Zeuglodon“) were found to be exceedingly common in southern states like Alabama, Richard Owen determining the fossil’s mammalian affinities only after Dr. Richard Harlan had deemed the remains to be reptilian and named the creature Basilosaurus. By 1845 enough material had been found and collected by Albert Koch to tour the country with a 114-foot-long skeleton of a “sea monster” named “Hydrarchos”, which was later revealed to be a composite monstrosity made from 5 different specimens of Basilosaurus and other species.
Koch’s “Hydrarchos”. Via Wikipedia.
“Hydrarchos”, the undignified beast. Via Interrogating Nature.
One of Charles R. Knight’s renditions of “Zeuglodon” (1913). From the book Monster Hunters
Given that Basilosaurus was discovered and brought to attention long before Darwin published On the Origin of Species, one would expect him to make some mention of it in the book, and indeed he does. On page 349 Darwin writes;
The cetaceans or whales are widely different from all other mammals, but the tertiary Zeuglodon and Squalodon, which have been placed by some naturalists in an order by themselves, are considered by Professor Huxley to be undoubtedly cetaceans, “and to constitute connecting links with the aquatic carnivora.”
From what I have been able to find, however, Darwin was unsure about whether “Zeuglodon” was an intermediate forms within the cetaceans, and he wrote to Huxley in October of 1871 to ask his friend’s opinion on the matter so that he might include a mention in the 6th edition of the book (which is the edition, I assume, that contains the above-quoted passage). Although the letters themselves are not yet online in their entiretly, it does appear that Huxley replied that there was little doubt of the connection between the ancient whales and living ones, whales probably being evolved from animals like living “carnivora” (dogs, cats, bears, civets, etc.). The problem is, however, that even though Basilosaurus showed differentiation in its teeth and greatly reduced hind limbs, it was still much closer in appearance to living whales than the ancestors of the group, only giving hints as to where to look. For almost 100 years the mystery of cetacean origins would remain.
In 1981 Pakicetus was named and described from fragmentary elements of the jaw and back of the skull by Philip Gingerich and Donald Russell , the parts of the skull that were recovered undoubtedly showing its cetacean affinities. This helped to fill in the story of cetacean evolution, and it seemed that the most likely candidates for the ancestors of whales were hoofed carnivorous mammals (“wolves with hooves”) named mesonychids. Still, the problem with Pakicetus was that so little of it had been found, and that for some time it was seen as something of a stubby proto-whale (see illustration above). Not until 2001, when more complete skeletons were found, were researchers able to have a look at the true form of the animal.
Regardless of whether whales evolved from artiodactyls or mesonychids (a controversy I’ll return to later), the discovery of the rest of the skeleton of Pakicetus is important as it gives us some clues as to how different animals might employ different strategies in returning to the water. Looking at the skeleton, Pakicetus was not a big, robust predator like a bear. It was far more like a dog or wolf (the reconstruction sometimes makes me want to say “rat on stilts”), the limbs and paws being relatively thin. Even though I’m sure Pakicetus could’ve doggie-paddled if it wanted to, this might not have been a very efficient or effective way at moving through the water, especially if you’re going to try and catch anything or use your mouth very much. Undulating the spine and using the limbs to give some extra push in moving the body forward would have been a more effective way to move for an animal that wanted to hunt in the water, and this is exactly the kind of motion we see in river otters (like these giant river otters at the Philadelphia Zoo) today;
This sort of stage in the aquatic evolution of cetaceans makes sense given the body plans of their ancestors, although it probably didn’t fully come into play until creatures like Ambulocetus or its descendants evolved. The precursor to the otter-like movement may have been something employed by other living mammals like muskrats, using the hind feet as the main propulsive appendages. Then again, muskrats and other mammals in rivers and lakes use various strategies to move through the water, so the ancestors of cetaceans probably went through a highly experimental stage before a certain type of locomotion started to be more firmly established.
As discussed earlier, mammals and their relatives were carrying their legs underneath their bodies and not out to the sides since the late Permian, and so the motion of their spine adapted to move in an up-and-down motion rather than side-to-side like many living reptiles and amphibians. Thus Pakicetus would not have evolved a tail for side-to-side motion like icthyosaurs or sharks because they would have had to entirely change the way their spinal column was set up first. At this point some of you might raise the point that living pinnipeds like seals and sea lions move in a side-to-side motion underwater. That may be true on a superficial level, but pinnipeds primarily use their modified limbs (hindlimbs in seals and forelimbs in sea lions) to move through the water; they aren’t relying on propulsion from a large fluke or caudal fin providing most of the propulsion with the front fins/limbs providing lift and allowing for change in direction. This diversity of strategies in living marine mammals suggests differing situations encountered by differing ancestors with their own suites of characteristics, but in the case of whales it seems that their ancestors were best fitted to move by undulating their spinal column and using their limbs to provide some extra propulsion/direction.
Sea Lion, taken at Sea World, Orlando (July 2006)
Looking at the vertebrae of icthyosaurs, sharks, and dolphins, it’s easy to see how mammalian vertebrae were modified to be useful for the mode of swimming exhibited by dolphins. Dolphins, unlike sharks and icthyosaurs, dolphins have two very large processes coming out of the sides of the vertebral centrum (the round part from which the processes branch), with another process sticking up fairly high. This increased surface area allows for much more muscle attachment than in sharks or icthyosaurs, being adapted to the up-and-down motion of the tail flukes. Early whales with increased surface area for muscle attachment along the spine for this kind of movement would be able to have more powerful tail strokes and probably move faster than others, natural selection modifying the spinal column of cetaceans to make the most of their arrangement. Also, the cervical vertebrae of many cetaceans are fused together, stabilizing the neck. If you’re going to be moving through the water with any amount of speed, it’d be a disadvantage to have a long neck with lots of joints that could be stressed or even broken by certain motions, so there would be an advantage in any move towards stability.
Even so, the skeletal specializations in modern cetaceans were just being formed back in the Eocene. Pakicetus, for example, appears as though it would have been a poor swimmer (as I had mentioned before), although its location makes it clear that it had an affinity for freshwater habitats. Also, the bones of Pakicetus seem to be compacted, thus making them relatively heavy, and some have thought that this condition could have acted almost like a diver’s weight belt or ballast (Thewissen & Williams, 2002). The next stage that we are aware of, exemplified by Ambulocetus, appeared to be much more at home in the water, although still far from its later relatives. Shifting towards shallow marine habitats (possibly bays or estuaries), Ambulocetus may have used its feet to swim through the water, and although some have suggested that it would have been too awkward to catch prey, I don’t think an Ambulocetus that actively hunted would be a foregone conclusion, especially if it swam with undulations of its spine as well as with its feet. Ambulocetus is also of interest in that it has characters in its lower jaw that relate to the lower jaw and ear morphology of living cetaceans, the lower jaw of dolphins being extremely important in receiving sounds during echolocation. Being that we know that the mammalian ear developed from the multiple jaw bones of their synapsid ancestors, it is easy to understand how the lower jaw and hearing mechanisms became so related in cetaceans and their ancestors.
There were various other varieties of archaeocetes, and later forms like Basilosaurus would take the successful early marine forms to extremes by adding and elongating their vertebrae, but I think vertebral undulation as a mode of swimming long preceded the known expression of this mode in the late Eocene whales like Dorudon and Basilosaurus. The evolution of modern whales from these forms is another story altogether (more of modifications of forms that were fully marine by that time), but once again we need to go back to the origins of this group to find some more controversy. A number of years ago, while I was still in elementary school, I remember seeing an episode of the TLC series “PaleoWorld” which featured whale evolution. The show definitely made the connection between mesonychid carnivores as being the ancestors to whales, showing one such creature (I assume it was a DinoMotion replica of Andrewsarchus peering contemplatively into a shallow pool). This seemed reasonable enough, Huxley’s idea of whales evolving from mammalian carnivores being somewhat vindicated, but then came a serious of important papers that shook up the phylogenetic tree.
What needs to be understood before we proceed, however, is that the change of ancestry from mesonychids to artiodactyls did not cause evolutionary theory to come crashing down. Mesonychids are closely related to both whales and artiodactyls, but in this case just being “close” doesn’t mean that they’re the right ancestors. To put this in perspective, the change of ancestry from mesonychids to artiodactyls isn’t nearly as big as the change from the hypothesis that birds evolved from pseudosuchian archosaurs like Ornithosuchus to the modern understanding that birds evolved from theropod dinosaurs. Even so, the changes have caused a good amount of controversy. The support for placing cetaceans within the clade Cetartiodactyla, with the hippopotamus and its relatives belonging to a sister group (mesonychids being just outside the new grouping). Morphological studies of the ankle bones and certain skull characters support this relationship as well, suggesting that living cetaceans and hippos shared a common, perhaps semi-aquatic, ancestor in their distant past.
But what happened to the hind limbs of cetaceans? If cetaceans evolved from land-dwelling ancestors, we would expect to see some change or vestige in the fossil record if not in living groups. In fact, that’s just what we have. While archaeocetes like Ambulocetus clearly still used their fore and hind limbs, by the time the group evolved into whales like Basilosaurus the hind limbs were greatly reduced, natural selection working towards eliminating the non-functioning appendages that would only increase drag. Although the reduction of the hind limbs in adults have been reduced or eliminated (save for a few cetaceans with atavisms like small pelvic fins or leg bones in their bodies in their pelvic region), the development of living cetaceans has also shown us that they once had another set of limbs. During development, dolphin embryos actually develop limb buds, but those that would normally become hind limbs or pelvic flippers stop developing and are reabsorbed into the body, showing that it’s not a matter of removing a trait but rather controlling it through development (which also explains the aforementioned atavisms now and then; sometimes the limb production goes forward, just at a stunted rate).
The relationship between cetaceans and artiodactyls (which encompass many groups of mammals like cows, pigs, giraffe, camel, deer, hippos, etc.) however, has cause some creationists to come up with some rather absurd illustrations in order to show evolution to be incorrect. No scientist that I know of is suggesting that a hippo turned into a whale or that a cow turned into a whale, unless you think cows looked something like Pakicetus (and I wouldn’t want to try milking one if I came across it on the shore of some Eocene lake).
My writing here is far from exhaustive or as in-depth as I would like (I need to learn some more physiology/anatomy, for certain), but I hope that I’ve given a fair superficial summation of how evolution can get from fish to tetrapod to whale, only a snippet of the evolution story of modern cetaceans that spans hundreds of millions of years. Even so, the journey out of the water and back into it, over and over again, is one of the most compelling evolutionary narratives known, especially given the intelligence and grace acheived by the descendants of some Eocene artiodactyls walking by the water’s edge.
Sea Lions that were playing “King of the Rock” at the National Zoo in Washington, D.C. (March 2007)
Bejder, L. and Hall, B.K. “Limbs in whales and limblessness in other vertebrates: mechanisms of
evolutionary and developmental transformation and loss” EVOLUTION & DEVELOPMENT 4:6, 445–458 (2002)
Buchholtz, E.A. “Vertebral osteology and swimming style in living and fossil
whales (Order: Cetacea)” J. Zool., Lond. (2001) 253, 175±190
Fish, F.E. “A mechanism for evolutionary transition in swimming mode by mammals” Secondary Adaptation of Tetrapods to Life in Water, J.-M. hlazin & V. de Buffrenil (eds.): pp. 261-287
Geisler, J.H. and Uhen, Md. “MORPHOLOGICAL SUPPORT FOR A CLOSE RELATIONSHIP BETWEEN
HIPPOS AND WHALES” Journal of Vertebrate Paleontology 23(4):991–996, December 2003
Gingerich, P.D. et al. “Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan” Science, 2239 (2001); 293
Gingerich, P.D. and Russel, D.E. “PAKICETUS INACHUS, A NEW ARCHAEOCETE (MAMMALIA, CETACEA) FROM THE EARLY-MIDDLE EOCENE KULDANA FORMATION OF KOHAT (PAKISTAN)” Museum of Paleontology, The University of Michigan, VOL. 25, NO. 11, p. 235-246
Milinkovich, M.C. “DNA-DNA hybridizations support ungulate ancestry of
Cetacea” J. evol. Biol. 5: 149-160 (1992)
Motani, R. “EVOLUTION OF FISH-SHAPED REPTILES (REPTILIA: ICHTHYOPTERYGIA) IN THEIR PHYSICAL ENVIRONMENTS AND CONSTRAINTS” Annu. Rev. Earth Planet. Sci. 2005. 33:395–420
O’Leary, M.A. “The Phylogenetic Position of Cetaceans: Further Combined Data Analyses, Comparisons with the Stratigraphic Record and a Discussion of Character Optimization” AMER. ZOOL., 41:487–506 (2001)
Thewissen, J.G.M. and Fish, F.E. “Locomotor Evolution in the Earliest Cetaceans: Functional Model, Modern Analogues, and Paleontological Evidence” Paleobiology, Vol. 23, No. 4. (Autumn, 1997), pp. 482-490.
Thewissen, J.G.M. and Williams, E.M. “THE EARLY RADIATIONS OF CETACEA (MAMMALIA): Evolutionary Pattern and Developmental Correlations” Annu. Rev. Ecol. Syst. 2002. 33:73–90
Watson, D.M.S. “The Evolution of the Mammalian Ear” Evolution, Vol. 7, No. 2. (Jun., 1953), pp. 159-177.