Friday, 21 August 2009

Whales - an Evolutionary Treasure Trove

Cetacea, the order that includes whales, dolphins and porpoises, has justifiably captured the imagination for millennia, from the scourge of Jonah to Moby Dick; Monstro the Great to Free Willy; we live in awe of them. It is common knowledge that dolphins show high intelligence and that blue whales (Balaenoptera musculus) are the largest animals to ever have lived, whales break more records than this; the sperm whale (Physeter catodon) can dive for longer and deeper than any mammal (10,000 ft); blue whales and fin whales (Balaenoptera physalus) produce the loudest sound in the animal kingdom (188 decibels); male humpback whales (Megaptera novaeangliae) produce the longest and most complex songs of any animal (up to 9 themes in half an hour, which it repeats for several days).

The plausibility of whale evolution has long been a source of fascination for scientists; and ridicule by creationists. Darwin speculated, to his own embarrassment, in the early editions of The Origin of Species:

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 aquatic in their structures and habits, with larger and larger mouths, till a creature was produced as monstrous as a whale.

Such speculation was justifiably rejected and whale evolution remained unsupported by tangible fossil evidence until recent decades. Who can forget Duane Gish’s comical “mer-cow” example of a half-cow, half-fish transition which he termed an “udder failure”? Bizarrely, cetaceans are still at the brunt of creationist attacks, when in actuality they present a wealth of evidence for evolution, not the supposed dearth.

First of all, is such a transition possible? Is a semi-aquatic life possible for a mammal? Visit any zoo or watch any good wildlife documentary (I recommend The Life of Mammals by David Attenborough) and you will find dozens of examples of different stages of amphibious life in extant mammals.

Mammals returning to the sea face many key problems: mammals need to keep warm, which aquatic life makes difficult; efficient movement requires different modifications to land movement; breathing air is difficult in the sea; giving live birth proves difficult under water. These obstacles have been conquered by both whales and many other mammals, but why bother? Food is often the key, and for whales in particular a niche was open; the mosasaurs, plesiosaurs and ichthyosaurs of the Mesozoic had all recently gone extinct, also meaning a lack of predation.

Living mammals provide examples of different stages of aquatic adaptation. In freshwater, the Desman (Desmana moschata and Galemys pyrenaicus) is an insectivore related to moles which has developed a flexible trunk-like snout for a snorkel, long dense fur for warmth and is a very effective swimmer. It remains tied to land as it is too buoyant to dive for long and must eat what it catches on land.

Sea otters (Enhydra lutris) spend all of their lives at sea, using their webbed toes for efficient propulsion. To keep warm they have the densest fur of any mammal, with more hairs in one square centimetre than any human has on their head, they even blow air into it for insulation. Sea otters mate in the sea and wrap themselves in kelp to stop from floating away whilst sleeping (they remain territorial).

Sea lions (of genera Eumetopias, Zalophus, Otaria, Neophoca and Phocarctos) take things further, with paddle-like front legs and back legs which are highly effective flippers yet still allow them to clumsily move on land. They have a lot of blubber and feed their young milk which is 30% fat in order to rapidly return to sea. They still give birth on land and have external ears.

Seals (of family Phocidae) lack the external ears, making them more streamlined. Their hind legs are shorter and cannot aid walking – they have to bounce around or slide when on land to give birth. Seals can stay submerged for up to 20 minutes.

All of these examples show different stages in adapting to the sea. Further discussion on each could be given, also including the fascinating manatees, but the point here is simply that a semi aquatic life is possible and therefore can lead to a fully aquatic one. Now onto the evidence from whales, but first, hippos.

Hippos (Hippopotamus amphibius) spend most of their time in the water and have many key adaptations to such a lifestyle. Their main sensory organs (eyes, ears and nose) are all atop their head allowing them to keep the rest of the body submerged; they are also able to tightly close them underwater. Mating occurs under water and the babies are born and suckle there too, even swimming before walking. A novel hippo adaptation is the secretion of their own sunscreen to prevent sunburn. I mentioned the hippopotamus last because molecular data shows them to be the closest relative of the cetaceans.

These extant examples show that it was at least possible and the molecular data should confirm that it did happen, but that is not enough for most, the fossils need discussing. We must confirm that it did happen with the visual tangibility that only fossils can provide; DNA often seems too abstract.

First comes Indohyus, an ancient artiodactyl the size of a raccoon. Dated to 48 million years ago it is not the ancestor of whales, but has features of the ears and teeth which are shared only by modern whales. It likely resembles the ancestor of whales and was partly aquatic, as evidenced by the denser bones and isotopic extractions from the teeth.

Next we turn to the famous Pakicetus from 52 million years ago. Pakicetus lacked the diving specialisations of modern whales and had intermediate teeth between mesonychids and archaeocetes. This ancestral whale was found in river sediments bordering an ancient sea, fitting for such a transition.

In this rapid trip through fossil whales (which does no justice to the evidence and misses some recent finds including the remingtonocetids such as Kutchicetus, the protocetid Maiacetus which gave birth on land, and many more) we turn to another famous fossil, Ambulocetus. Fifty million years ago the sea lion sized Ambulocetus spent most of its time in shallow water using flippers which still had vestigial hooves. The most important feature of Ambulocetus is the spine – it was highly flexible, allowing for up and down undulations which led to the distinctive locomotive style of all cetaceans.

Many fossils show more progression, such as Dalanistes with its still fully functional limbs with webbed feet and its long snout. Both Indocetus and Rodhocetus (46.5 mya) were partly terrestrial (though very limited) and highly agile in the water. The nostrils of Rodhocetus had moved back – the start of the transition to the blowhole. Other fossils showing more progression include Takracetus and Gaviocetus (both have vestigial hind limbs) and more will undoubtedly be found.

On the whale side of the transition are Basilosaurus and Dorudon from 40 mya. Both had short necks and their blowholes were atop the skull. They also had tiny hind limbs, useless for land locomotion yet still present. These were around 2 foot long on a 50 foot whale and included all the usual hind limb bones including the patella and phalanges.

The fossils show an incredible sequence, one which stretches incredulity to doubt (I recommend looking at them and not relying on my short descriptions). This brief overview gave only a glimpse, the fossils, when studied in more detail, show how almost every unique whale feature evolved, from the blowhole to their locomotion. In almost all cases this required modification of existing traits. As fossils are discussed so often when covering whale evolution I will turn to other lines of evidence.

One of my favourite pieces of evidence for evolution is the presence of pseudogenes, and whales do not disappoint. The olfactory receptor (OR) genes are an important and fascinating group of genes, the elucidation of which won the Nobel Prize for Axel and Buck in 2004.

The OR genes originated from a single gene which has been duplicated repeatedly and altered slightly each time. Their number correlates with the strength of the sense of smell of the animal (an unusual occurrence with genes). A brief look at them in a variety of species is illuminating. Many ‘primitive’ fish have 2 sets of OR genes, lobe finned fish use only one of these sets, homologous to the set used in terrestrial animals. Fish have just a handful of OR genes, amphibians tend to have more, reptiles even more so and mammals can have over 1,000. Already a sequence has emerged.

Looking at mammals more closely, those that rely heavily on smell, such as the mouse or dog, have the full complement of OR genes, all in use. Our own sense of smell is a lot weaker, using only around 400 OR genes. We still carry around 800 OR genes – half have become pseudogenes and are inactive. This coincides with our dependence on colour vision, relying less on smell (which usually leads into another of my favourite examples of evolution).

With this information a prediction can be made. If cetaceans evolved from terrestrial mammals they should have hundreds of OR genes, though as their nose is now a blowhole they should largely be inactive. A look at the dolphin genome shows that 80% of their OR genes are inactive. They also resemble the usual mammalian OR genes. This makes proper sense only in light of the theory of evolution.

Pseudogenes are the genetic equivalent of vestigial traits, which whales also have. Whales famously have a vestigial pelvis and thigh bones which serve little to no purpose except as a pointer to their evolutionary heritage. Occasionally (1 in 500) whales have atavistic legs which protrude outside the body wall, many containing leg bones, some even having feet and toes!

The most exciting discoveries being made in current evolutionary biology come from the study of embryological development and the pathways taken. In a 24 day old spotted dolphin (Stenella attenuata) embryo there is a well developed hind limb bud, only slightly smaller than the forelimb bud. By 48 days the hind limb buds have mostly been reabsorbed whilst the forelimbs continue to develop into flippers. Baleen whales, which are toothless, develop embryonic teeth which are also reabsorbed before birth.

Another example is present in human development too. Foetal humans of around 6 months develop fine, downy hair called lanugo. Lanugo is shed around a month before birth in humans, whereas other apes retain it. Foetal whales also develop lanugo and shed it before birth. These embryonic examples hint at their descent from four-limbed, fur covered ancestors.

More detailed study has been done into the genetic basis of the embryological development of cetaceans, proving to be most illuminating.

Whales still have the main genes used in limb formation (Shh, the Fgfs and Hand2) though the regulation has changed. A loss of the genes would not be possible (it would hinder other areas of development) so their activation was selectively reduced. The changes have been pinpointed to the expression of Hand2, being expressed in the forelimb and not the hind, forming no zone of polarising activity (ZPA) for that limb, thus halting formation. The evidence suggests this shutting off occurred approximately 34 mya.

At the same time the limbs were lost there was a change in vertebral patterning. Hox expression (Hoxd) appears to have altered both features, effecting Shh and Hand2 expression. Not only can we observe fossils, development also shows exactly which mutations may have occurred.

Whales and other cetaceans are not only awe inspiring to observe, they also provide incredible evidence and insights into evolution. The small amount presented here scratches the surface and displays a confluence of disparate evidences from various separate disciplines which are made sense of by the theory of evolution.

References and recommended reading (in non-scientific format):

The Encyclopedia of Animals - published by Weldon Owen (2008).

The Life of Mammals (DVD) – David Attenborough (2002).

Why Evolution is True – Jerry Coyne (2009).

Evolution: What the Fossils Say and Why It Matters – Donald Prothero (2007).

Hooking Leviathan By Its Past, from Dinosaur in a Haystack: Reflections in Natural History – Stephen Jay Gould (1995).

Your Inner Fish – Neil Shubin (2008).

The Origin of Whales and the Power of Independent Evidence:

Inclusion of Cetaceans Within the Order Artiodactyla Based on Phylogenetic Analysis of Pancreatic Ribonuclease Genes:

Molecular evidence for the inclusion of cetaceans within the order Artiodactyla:

Molecular evidence from Retroposons that whales form a clade within even-toed ungulates:

Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls:

From Land to Water: the Origin of Whales, Dolphins, and Porpoises:

Whales originated from aquatic artiodactyls in the Eocene epoch of India:

Fossil Evidence for the Origin of Aquatic Locomotion in Archaeocete Whales:;263/5144/210

Vestibular evidence for the evolution of aquatic behaviour in early cetaceans:

New Protocetid Whale from the Middle Eocene of Pakistan: Birth on Land, Precocial Development, and Sexual Dimorphism:

A remarkable case of external hind limbs in a humpback whale:

Limbs in whales and limblessness in other vertebrates: mechanisms of evolutionary and developmental transformation and loss:

The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans:

Whale limb evolution:

Sound transmission in archaic and modern whales: Anatomical adaptations for underwater hearing:

Eocene evolution of whale hearing:

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