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Home , Ambulocetus, Dorudon, Hans Thewissen, Indohyus, Pakicetidae, Pakicetus

NOT FOR SALE

The earliest whales, such as the 47-million-year-old Ambulocetus, still had legs. Their anatomy gives us clues to how whales made the transition from land to sea.

ne of the best feelings paleontologists can ever

have is to realize that they’ve just found a fossil

that will fll an empty space in our understanding Oof the history of life. Hans Thewissen got to enjoy that feeling one day in 1993, as he dug a 47-million-year-old fossil out of a

hillside in Pakistan. As he picked away the rocks surrounding the FIGURE 1.1 bones of a strange mammal, he suddenly realized what he had Paleontologist Hans Thewissen has discovered many of the bones of found: a whale with legs. Ambulocetus in Pakistan.

A hundred million years ago, not a single whale swam in all

the world’s oceans. Whales did not yet exist, but their ancestors

did. At the time, they were small, furry mammals that walked on

land. Over millions of years, some of the descendants of those

ancestors underwent a mind-boggling transformation. They lost

their legs, traded their nostrils for a blowhole, and became crea-

tures of the sea. This profound change was the result of evolution.

3 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOTThis bookFOR is an introduction to that SALE process. Over the course of some 3.5 billion years, life has evolved from humble beginnings into the tremendous diversity found today on Earth—from whales to tulips to viruses. Indeed, to understand life on Earth—its diversity of forms, of biochemistry, of behav- iors—it’s crucial to understand evolution. The great twentieth-century biologist Theodosius Dobzhansky summed up the importance of this branch of science in 1971 when he declared, “Nothing in life makes sense except in the light of evolution” (Dobzhansky 1973). The Tangled Bank is intended for anyone with a curiosity about how life works. To explain mathematical concepts, for example, it uses graphs and diagrams rather than detailed equations. This book presents the research of scientists like Thewissen not in technical detail, but through their own experi- ences of discovery. When Charles Darwin formulated the theory of evolution in the mid-1800s, the most sophisticated tool he could use was a crude light microscope. As we’ll see in this book, scientists today can study evolution in many ways—by analyzing our DNA, for example, by probing the atoms of ancient rocks to determine the age of fossils, or by programming powerful com- puters to decipher how a thousand diferent species are related to each other. Understanding evolution is too important to be limited only to evolutionary biologists. Evolution underlies many important issues society faces, and a better understanding of evolution can help us to grapple with them. The world’s biodiversity faces many threats, from deforestation to global warming. By studying past mass extinctions, we can better understand our current crisis. Evolution has produced bacteria that can resist even the most powerful antibiotics. Scientists can observe this resistance as it evolves in laboratory experiments. The evolution of pests and pathogens poses a serious risk to our food supply. But evolution can also help us to address some of the biggest questions we ask about the universe and ourselves: How did we get here? What does it mean to be human?

What Is Evolution? The short answer is descent with modifcation. The patterns of this modifcation, and the mechanisms by which it unfolds, are what evolutionary biologists study. They have much left to learn—but at this point in the history of science, there is no doubt that life has evolved and is still evolving.

4 CHAPTER 1 | WALKING WHALES © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES TheNOT fundamental principles that makeFOR evolution possible are prettySALE straightforward. Organisms inherit traits from their ancestors because they receive a molecule called DNA from them (see page tk for a discussion of heredity). Cells use DNA as a guide to building biological molecules, and, when organisms reproduce, they make new copies of DNA for their offspring. Living things do not replicate their DNA perfectly; sometimes sequence errors occur. Such errors are referred to as mutations (Chapter 5). A mutation may be lethal; it may be harmless; or it may be benefcial in some way. A benefcial mutation may help an organism to fght off diseases, to thrive in its environment, or to improve its ability to fnd mates. Evolution takes place because mutated genes become more or less common within populations over the course of generations. Many mutations even- tually disappear, while others spread widely. Some mutations spread simply by chance. Others spread because they allow organisms to produce more offspring. This nonrandom spread of benefcial genes is known as natural selection. The effect of a mutation depends on more than just the mutation itself. It is also infuenced by all the other genes an organism carries. The environment in which an organism lives can also have a huge effect. As a result, the same mutation to the same gene may be harmful in one individual and harmless in another. Natural selection may favor a mutation in one set of circumstances and may drive it to oblivion in another. These processes are taking place all around us every day, and they have been accumulating genetic changes ever since life began at least 3.5 billion years ago (Chapter 3). Darwin argued that over such vast stretches of time, natural selection could have produced complex organs, from the wings of birds to human eyes. Today, the weight of evidence overwhelmingly supports that conclusion. Changes in organs are not the only adaptations that have emerged through evolution; behavior and even language have evolved as well (Chapters 13 and 14). To trace the history of these traits, evolutionary biologists reconstruct how species diverged from a common ancestor (Chapter 4). Natural selection and other processes can make populations genetically distinct from one another. Over time, the populations become so different from one another that they can be considered separate species (Chapter 9). One way to picture this process is to think of the populations as branches on a tree. When two populations diverge, a branch splits in two. As the branches split again and again over billions of years (and sometimes came back together), the tree of life emerged. To reconstruct the tree, evolutionary biologists identify which species are closely related to each other. They do so by comparing anatomical traits and DNA among many different species. Close relatives share more traits inherited from their common ancestor. We humans have a bony skull, for example, as do all other mammals, as well as birds, reptiles, amphibians, and fshes (Chapter 4). We are more closely related to these animals than we are to animals without a skull, such as earthworms and ladybugs. Evolutionary biologists investigate not only adaptations, but the shortcom- ings of those adaptations. Life does not evolve by steadily progressing toward some particular goal. Our apelike ancestors did not evolve big brains because they “needed” them, for example; the conditions in which they lived—search- ing for food on the African savanna in big social groups—were such that some traits were favored over others (Chapter 14). Our ancestors benefted from a bigger, more complex brain, but in some ways it’s a spectacularly maladapted organ. The human brain is so big that it makes childbirth much more danger- ous for human mothers than for other female primates, for example. It also

WHAT IS EVOLUTION? 5 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOTrequires a hugeFOR amount of energy to supply—oneSALE out of every fve calories you eat is used to fuel your brain. Evolution is imperfect, because it does not invent things from scratch: it only modifes what already exists. Any organism can acquire only a limited number of benefcial mutations, and so evolution can produce new forms only under tight constraints. Because mutations can have several different effects at once, evolution also faces trade-offs. Mutations that increase the number of offspring an organism can have may also cut down its life span. These tradeoffs underlie some of the diseases that are common in the elderly, such as cancer. As a result, studying evolution can help researchers better understand—and perhaps even treat—these diseases (Chapter 15). Evolution has produced many helpful partnerships in nature, such as the one between fowering plants and the insects that pollinate them—a partner- ship we depend on for many of our crops (Chapter 12). But evolution does not produce a peaceful balance in the natural world. The same process species use in adapting to one another can also give rise to what looks to us like cruelty. Pred- ators are exquisitely adapted to fnding and killing prey. Parasites can devour their hosts from the inside out. Their adaptations are fnely honed, allowing them to manipulate individual molecules within their hosts. Yet parasites and predators are not evil. They are just part of a dynamic balance that is constantly shifting, driving the diversifcation of life but also leading to extinctions. The diversity of nature, in other words, is not eternally stable. More than 99 percent of all species that ever existed have become extinct, and, at some points in Earth’s history, millions of species have disappeared over a relatively short span of time. We may be at the start of another period of mass extinctions, this time caused by our own actions (Chapter 11).

A Case of Evolution: Why Do Whales Have Blowholes? Evolutionary biology is a science of integration. To investigate questions about life, evolutionary biologists integrate evidence from many different sources, gathered with many different methods. Throughout this book, I take a close look at many examples of scientists weaving together different pieces of research to understand evolution. These examples run the gamut, from venom- ous snakes to drug-resistant bacteria. But there’s no better way to launch an exploration of evolution than by looking at whales and dolphins (FIGURE 1.2). Charles Darwin, who established the major concepts of evolution in his 1859 book The Origin of Species, was the frst evolutionary biologist to think about how whales evolved. He recognized that living whales and dolphins (known collectively as cetaceans) are a biological puzzle. They have fsh-like bodies, sculpted with the same sleek curves you can fnd on tunas and sharks, so they use relatively little energy to shoot through the water. The tails of whales and dolphins narrow down to a small neck and then expand into fattened fukes, which they lift and lower to generate thrust. Sharks and tunas have similar tails, but they move theirs from side to side. Despite their fsh-like appearance and ecology, however, cetaceans are different from fshes in some profound ways. To breathe, for example, they must rise to the surface of the ocean. Then a blowhole on the top of the head opens and draws air into a passageway leading to their lungs. Most fsh species can get all the oxygen they need by pumping water through their gills, where

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FIGURE 1.2 Living whales all share a number of traits, such as blowholes and Other species, such as killer whales (center) and dolphins (right), horizontal tail fukes. Some species have flter-like growths in their have peg-shaped teeth that they use to grab larger prey such as fsh mouths that they use to sieve small animals from seawater (left). and seals.

some of the dissolved oxygen passes into their blood vessels. Cetaceans have tiny bones embedded in their fesh just where the hips would be on a land vertebrate. Fishes have relatively simple sets of muscles that form vertical blocks from head to tail, whereas whales and dolphins have long muscles that run the length of their bodies—much like the long muscles running down your back. Cetaceans give birth to live young that cannot get their own food; instead, they must drink milk that their mothers produce with special mammary glands. Together, these differences make cetaceans utterly unlike fshes. The only group of species where you can fnd such a combination of traits is mammals. Darwin proposed a straightforward explanation for this puzzling pattern of similarities and differences. Cetaceans descended from mammals that lived on land, and their lineage evolved into marine mammals through natural selection. The ancestors of modern whales lost their hindlimbs, and their front legs became shaped like fippers. But today whales still have many traits they inherited from their mammalian ancestors, such as lungs and mammary glands. Evolution, as Darwin envisioned it, was a gradual process. A land mammal did not give birth to a full-blown whale, in other words. If Darwin was right about this, then intermediate species of cetaceans must have existed in the past. These transitional forms would have started out being adapted to life on land and then gradually adapted to water instead. But Darwin could not point to such a fossil record, because in the mid-1800s, paleontologists were only starting to dig up extinct cetaceans. When Darwin died in 1882, he was not much wiser about how cetaceans evolved. The frst cetacean fossils paleontologists discovered were already completely adapted to life in the water. Dorudon, a species that lived 40 million years ago, is a typical example of these ancient cetaceans (FIGURE 1.3). Its fippers and long vertebral column were very much like those of living cetaceans. The most compelling evidence that Dorudon was a cetacean was far subtler, however. The mammalian middle ear is an air-flled cavity enclosed in a hollow shell. Whales and dolphins have this same structure, but with some distinctive features. On one edge of the shell is a thick lip of dense bone, called the involucrum. In no other group of mammals do scientists fnd an involucrum. Dorudon has an involucrum—providing strong evidence that it’s a cetacean (Thewissen et al. 2009). In other ways, however, Dorudon was also different from any living cetacean. Consider its teeth. Dorudon had incisors in the front and molars in the

A CASE OF EVOLUTION: WHY DO WHALES HAVE BLOWHOLES? 7 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOT FOR SALE Incisors and canines aligned with cheek teeth

Narrow postorbital/ temporal region

Bulla

Lateral view

Bulla

Ventral view Dorsal view

FIGURE 1.3 In the late 1800s, paleontologists began to discover early whales, On the other hand, Dorudon also had some traits not found in such as Dorudon, a 5-meter-long whale that lived 40 million years living species, including a blowhole midway up its snout and com- ago in Egypt. Dorudon was a completely aquatic whale and had a plete hind legs (albeit very small ones). Living whales have cone- number of traits found today only in living whales, such as the tooth shaped teeth, while Dorudon had more complex ones that resemble and skull features noted in this fgure. The grape-shaped bone those of certain extinct land mammals. This combination of traits called the bulla contains bones of the middle ear; some anatomical refects Dorudon’s transitional position in the evolution of whales. features within the bulla of Dorudon are also shared by living whales. (Adapted from Uhen 2010.)

back. Each tooth had a complex set of cusps and ridges. No living whale has anything like this dental arrangement. One group of cetacean species, known as odontocetes, has simple cone-shaped teeth. The other cetaceans, known as mysticetes, have no teeth at all: instead, they flter out small animals through baleen. The teeth of Dorudon are actually much more similar to those of land mammals than of living cetaceans. This trait could well be the result of the gradual evolution of whales: long after the rest of their body had evolved many adaptations to the water, early whales still had teeth like terrestrial mammals. Cetacean evolution started to come into much sharper focus in the late 1970s. At the time, Philip Gingerich—a young paleontologist from the Univer- sity of Michigan—was paying regular visits to Pakistan to investigate a geo- logical formation from the Eocene period, 56 million to 34 million years ago. Gingerich wanted to document the mammals that existed in that region during that time. He and his colleagues brought back a number of fossils to Michigan and then slowly prepared them in his laboratory, extracting the fossilized bone from the surrounding rock. One 50-million-year-old fossil—the teeth and back portion of a wolf-sized skull—was particularly intriguing. It bore some strik- ing similarities to cetaceans such as Dorudon, especially in its teeth. Gingerich concluded that he had found the earliest known cetacean, which he and his colleagues dubbed Pakicetus (Gingerich, Rose, and Krause 1980).

8 CHAPTER 1 | WALKING WHALES © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES Gingerich’sNOT discovery was dramatic FOR not just for the great ageSALE of the fossil but also for where he had found it. Whales and dolphins today live only in the water—most live in the ocean, and a few species of dolphins live in rivers. The rocks in which Pakicetus fossils formed offer clues to the environment in which it lived. Geologists have determined that those rocks formed as sediment accumulated in shallow streams that fowed only seasonally through a hot, dry landscape (Thewissen et al. 2009). This evidence strongly suggests that Pakice- tus lived on land (FIGURE 1.4). Gingerich’s discovery was the frst of a dazzling number of ancient cetacean fossils that have come to light over the past 30 years. One of the most important was discovered by Thewissen, who studied with Gingerich in the late 1980s. As part of his graduate school research, Thewissen traveled to a different part of

C Involucrum

Middle ear cavity

Fossil Pakicetus Dolphin Lagenorhynchus

FIGURE 1.4 A: The 50-million-year-old Pakicetus was the frst terrestrial whale ever discovered. This reconstruction is based on fossils from several diferent individuals. The fossil material is colored red. B: A painter’s reconstruction of what Pakicetus looked like in life. C: Pakicetus bears certain hallmarks found in only cetaceans and no other mammals. On the right is a bone (from a dolphin) called the ectotympanic. It is located in the bulla, which surrounds the middle ear cavity. In living cetaceans, the inner wall of the ectotympanic forms a thick, dense lip called the involucrum. On the left is the ectotympanic from Pakicetus. It has a similar involucrum. Such uniquely shared traits reveal that Pakicetus was an ancient relative of living whales and dolphins. (Adapted from Cooper et al. 2009; Gingerich et al. 1983; Luo and Gingerich 1999; Nummela et al. 2006; Thewis- sen et al. 2009.)

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FIGURE 1.5 The skeleton of Ambulocetus shares the hallmarks found today only in whales, such as an involucrum. It was also the frst fossil whale ever discovered with complete legs. A reconstruction of Ambulocetus is shown on page 2.

Pakistan to look for mammals that lived a few million years after Pakicetus. One day Thewissen and his Pakistani colleagues happened across a strange fossil of a large mammal. They slowly excavated its bones from the tail to the head. Its tail was massive, its legs were stubby, and its rear feet were shaped like paddles. Even as Thewissen was digging up the fossil, he could see that its head was long like an alligator’s, but it had teeth like those of fossil whales (FIGURE 1.5). Thewissen brought the fossil to the United States, where he continued preparing and analyzing it. He discovered more traits linking it to cetaceans, including a thickened involucrum. He concluded that the fossil was, in fact, a whale that could walk. He named it Ambulocetus: “walking whale” (Thewissen et al. 1997; Zimmer 1998). A reconstruction of Ambulocetus can be found on the opening page of this chapter. In the years that followed, paleontologists found many fossils of different species of whales with legs. Thewissen, who now teaches at Northeast Ohio Medical University, has found additional bones of the older cetacean ancestor Pakicetus. Fragments of its skull revealed it to have a cetacean-like involucrum and also showed that its eyes would have sat on top of its head (see Figure 1.4). Fossil bones from other parts of its skeleton have led Thewissen to reconstruct Pakicetus as a wolf-sized mammal with slender legs and a pointed snout. Gingerich, meanwhile, found the fossils of another cetacean called Rodhocetus, whose short limbs resembled those of a seal. As the evidence that cetaceans evolved from land mammals grew, scientists wondered which group of land mammals in particular they had evolved from. One way to address this question is to compare the DNA in living species. As we’ll see in Chapter 7, scientists can use genetic information to draw evolutionary trees showing the relationships between species. In the 1990s, several research groups began comparing snippets of DNA from cetaceans and other mammals. They concluded that those species were most closely related to a group of mammals called artiodactyls, which includes cows, goats, camels,

10 CHAPTER 1 | WALKING WHALES © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOT FOR SALE A

Astragalus

ox (Bos)

B Astragalus (ankle bone)

1 cm

Indohyus Pakicetus pig (Sus) deer (Odocoileus)

FIGURE 1.6 A: Artiodactyls are a lineage of mammals that includes cows, hippos, and girafes. All artiodactyls have an ankle bone, called the astragalus, with a distinctive double-pulley shape. B: The astragali of two living artiodactyls are shown here next to the fossil astragali of two ancient whales. The double-pulley shape of these bones is evidence that whales evolved from artiodactyls on land (Thewissen et al. 2009). and hippos. As they compared more DNA from these species, the cetacean- artiodactyl link only strengthened. In fact, the scientists concluded that cetaceans were most closely related to hippos (Price, Bininda-Emonds, and Gittle- man 2005). This conclusion was a hypothesis, and like all good hypotheses, it could be tested. All living and fossil artiodactyls, for example, share a distinctive ankle bone called an astragalus. Unlike any other mammal, artiodactyls have an astragalus with an end shaped like a pulley (FIGURE 1.6). If cetaceans did

A CASE OF EVOLUTION: WHY DO WHALES HAVE BLOWHOLES? 11 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOT FOR SALE 55 50 45 40 35 30 25 Millions of years ago

Hippopotamus

Indohyus

Pakicetus

Involucrum Freshwater semiaquatic habitat Ambulocetus

Kutchicetus

Large, powerful tail Shorter legs Fat pad in jaw for hearing Rodhocetus Brackish water habitat

Saltwater habitat Dorudon

Nasal opening shifted back Eyes on side of head

Odontocetes Tail fukes Very small hind legs Nasal opening shifted further back

Complete loss of hind legs Nasal opening reaches position of blowhole in living whales

Echolocation for hunting Mysticetes

Baleen for fltering food

FIGURE 1.7 The relationship between some extinct species of early whales and living species. The animals illustrated here are only a fraction of the fossil whales that paleontologists have discovered in recent decades. By studying fossils, paleontologists have been able to show how the traits found in living whales evolved gradually rather than all at once.

12 CHAPTER 1 | WALKING WHALES © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES indeed NOTevolve from an artiodactyl, thenFOR the early cetaceans that SALE still had feet should bear a double-pulley astragalus. As it happens, this small bone is rarely preserved in a fossil. But Thewissen and Gingerich both discovered the bone on ancient cetaceans—and, in both cases, it was indeed pulley shaped. To see how cetaceans evolved from artiodactyls, it helps to draw the evolutionary relationships between species. As shown in FIGURE 1.7, such an image can take the form of a tree. Each line in the tree represents a lineage reproduc- ing through time; lineages split to produce new ones. We have some clues about the age of these lineages from different kinds of evidence, such as fossils. The thick lines in Figure 1.7 show lineages that are documented in the fossil record; the thin lines, the lineages we can infer from the evidence. (In Chapter 4, we’ll explore these trees and how to interpret them in more detail.) The earliest cetaceans, such as Indohyus and Pakicetus, had four legs. They may have been able to swim, but only by kicking their legs like many land mammals—like hippos—do today. From such terrestrial ancestors, other lineages evolved that were more adapted to life in water. Ambulocetus lived about 49 million years ago along the coastline of what is now Pakistan. It had short legs and massive feet. Its skeleton suggests that it swam like an otter, kicking its large feet and bending its tail. Rodhocetus, with its seal-like limbs, probably could only drag itself around on land. The pattern of evolution in the fossil record suggests that natural selection favored adaptations, such as short legs, that made cetaceans more effcient at swimming in water. But evolution did not completely retool cetaceans from the ground up. Cetaceans did not evolve gills, for example. Instead, the phylogeny of cetaceans indicates that their nostrils gradually shifted up to the top of their skulls, allowing them to take in air more effciently each time they rose to the surface of the water. Cetacean fossils also show that the loss of hind legs took millions of years. Some 40 million years ago, fully aquatic species such as Dorudon had evolved. But Dorudon still had small but complete hindlimbs. (A related cetacean of the same age, called Basilosaurus, provides an even more spectacular demonstration of this evolutionary lag: it grew to the size of a school bus, and yet had hind legs, complete with ankles and toes, the size of a young child’s.) The embryos of living cetaceans offer some clues about how cetaceans lost their legs. Legs arise in mammal embryos as a distinctive set of genes become active at one end of the embryo. Hans Thewissen, collaborating with a team of embryologists, discovered that these same genes also become active in dolphin embryos. Tiny buds of tissue sprout from the fanks of the dolphin embryo as they do in other mammals (FIGURE 1.8). But these limb buds stop growing after a few weeks and then die back. The study by Thewissen and his colleagues points to a compelling hypothesis for how whales lost their legs: mutations arose that could stop the growth of the limbs shortly after they had started forming (Thewissen et al. 2006). In Chapter 8, we’ll see how this kind of evolutionary change to development has helped produce life’s diversity. The early cetaceans evolved into many lineages, most of them long extinct. The odontocetes and mysticetes, the two lineages of cetaceans still in existence today, split from a common ancestor about 40 million years ago. After that split, the odontocetes evolved muscles and special organs that they used to produce high-pitched sounds in their nasal passages leading to their blowholes. Listen- ing to the echoes that bounced off objects around them in the water, they could perceive their surroundings. Today, dolphins and other odontocetes use these echoes to hunt for their prey. The mysticetes followed a different trajectory:

A CASE OF EVOLUTION: WHY DO WHALES HAVE BLOWHOLES? 13 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOT FORWeeks 4–9 of embryonicSALE development

Forelimb

Hindlimb

FIGURE 1.8 A dolphin embryo grows buds of both forelimbs and hindlimbs. The forelimb buds go on to de- velop into fns. The hindlimbs, on the other hand, are absorbed back into the embryo. Scientists have found that simple changes in the timing of gene expression have helped transform early terrestrial whales into their fsh-like descendants (Thewissen et al. 2009).

They didn’t evolve echolocation. Instead, they lost their teeth and evolved huge, stiff pleats in their mouths that allowed them to flter prey from huge volumes of water. Scientists are now beginning to fnd important new clues to the origins of both groups. Fossils have revealed that the earliest mysticetes still had teeth, for example, and probably grew only small patches of baleen at frst (Uhen 2010). Only later did their teeth disappear. Mysticetes still carry genes for building teeth, but most of them have acquired disabling mutations. Biologists have long been impressed with the size and complexity of whale brains (FIGURE 1.9). Aside from humans, dolphins have the biggest brains in proportion to their bodies of any animal (Marino 2007). Dolphins can also use their oversized brains to solve remarkably complicated puzzles that scientists make for them. A number of studies suggest that big brains evolved in dolphins as a way to solve a particular kind of natural puzzle: fguring out how to thrive in a large social group. Dozens of dolphins live together, forming alliances, competing for mates, and building relationships that persist throughout their long lives. They communicate with each other with high-frequency squeaks, and each dolphin can tell all the other dolphins apart by their whistles. Natural selection appears to have favored dolphins with extra brainpower for process- ing social information (Connor 2007). One of the big lesson of the fossil record is that groups of species rise and fall in diversity over evolutionary times (Chapter 11). Cetaceans are no excep- tion. Mark Uhen, a paleontologist at George Mason University, recently tallied the diversity of cetaceans over the past 50 million years, and his research chron- icles dramatic fuctuations in the number of species (FIGURE 1.10; Uhen 2010). There are many such patterns in the fossil record, and evolutionary biologists are testing hypotheses to explain them. Uhen has argued that cetacean evolution kicked off with an explosion of semiaquatic species such as Ambulocetus. By the end of the Eocene, however, fully aquatic forms like Basilosaurus had evolved, and the semiaquatic forms had become extinct (Uhen 2010). The fully aquatic cetaceans became top predators in the ocean ecosystem. The two living lineages of cetaceans evolved very different strategies for hunting: the mysticetes trapped small animals with their baleen while the odon-

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Human (Homo sapiens) 5 cm

Bottlenose dolphin (Tursiops truncatus)

FIGURE 1.9 A: Dolphins live in large groups and can communicate to each other favored the evolution of big, powerful brains. Relative to their body with complicated sounds. B: Their complex social life may have size, dolphin brains are second only to those of humans.

tocetes swam after fshes and larger prey. But in both cases, they depended on productivity of the ocean food web for their food. Uhen and Felix Marx of the University of Bristol have observed that cetacean diversity shot up after large, shelled algae called diatoms became diverse in the ocean starting about 20 million years ago (Marx and Uhen 2010). Uhen and Marx argue that the explosion of diatoms provided a food supply for animals that in turn were preyed upon by a diversity of cetaceans. Unfortunately for cetaceans, a new predator has entered their lives in the past few centuries: humans. In the 1800s, sailors crisscrossed the world to hunt big whales for their oil and baleen (the oil was used for lamps and the baleen for corset stays). Many species of whales came perilously close to extinction before the whale-oil industry collapsed and laws were passed to protect the surviving animals (FIGURE 1.11). Whales reproduce slowly, and so their populations are still far from their pre-hunting levels. The small sizes of their populations put them at a greater risk of extinction. Diseases and other threats, such as pollution and heavy fsh- ing, can destroy large fractions of small populations more readily than big ones. Small populations also have little genetic variability, making them more susceptible to genetic disorders (Chapter 6). In the 1950s, for example, an estimated 6000 Chinese river dolphins (Lipotes vexillifer) lived in the Yangtze River (FIGURE 1.12). But the booming Chinese economy led to massive pollution of the river, sickening the animals. Fishermen killed many of them by accident in their nets. Because of these human activi- ties, the Chinese river dolphin population began to crash; in 1997, an extensive search revealed only 13 individuals. And the last Chinese river dolphin was

A CASE OF EVOLUTION: WHY DO WHALES HAVE BLOWHOLES? 15 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOT FORBalaenoptera SALE (middle Miocene to recent) 80 Modern diversity 70

Llanocetus 60 (Eocene/Oligocene boundary)

Dorudon 50 (late Eocene)

30 Georgiacetus (middle Eocene) Number of cetacean genera

0 Bartonia Priabonian Aquitania Bu Langhia Serravallian T Messinia Zanclean Piacenzian Gelasian ortonia rd

Ypresian Lutetian Rupelian Chattian igalia n n n n n n Pleistocene E M LEE L E M L L Holocene Eocene OligoceneMiocene Plio- cene

55.8 mya PALEOGENEN33.9 23.0 EOGENE 5.3 1.8

FIGURE 1.10 The fossil record of whales documents increases and decreases in the ocean’s ecosystems have driven these long-term changes (Uhen the diversity of species over the past 55 million years. Paleontolo- 2010). gists have hypothesized that changes in the planet’s climate and

FIGURE 1.11 Whale hunting in the nineteenth century nearly drove many species of whales extinct. They have been rebounding slowly, although today they continue to face many threats from human activity.

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FIGURE 1.12 The Chinese river dolphin (Lipotes vexillifer) is believed to have become extinct in recent years due to pollution and overfshing.

spotted in the river in 2007 (Turvey 2009). It’s possible that a few dolphins are surviving somewhere along the Yangtze; but with each passing year, it is more likely that these remarkable creatures have become extinct and will never be seen again. Even as we humans have come to understand the remarkable history of cetaceans over the past 50 million years, their future evolution has ended up in our hands. Most people fnd whales and dolphins awe-inspiring the moment they set eyes on these remarkable animals. Learning about the evolution of whales and dolphins only deepens their fascination. By probing the history of life—of cetaceans and the millions of other species we share this planet with—we can come to understand the tapestry of change that has been weaving itself for billions of years. Charles Darwin put it best with the closing lines of The Origin of Spe- cies: “There is a grandeur in this view of life, with its several powers, having been breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fxed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being evolved.”

A CASE OF EVOLUTION: WHY DO WHALES HAVE BLOWHOLES? 17 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES NOTFurther FOR Reading SALE Barton, N. H., D. E. Briggs, J. A. Eisen, D. B. Goldstein, and N. H. Patel. 2007. Evolution. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Coyne, J. A. 2009. Why Evolution Is True. New York: Viking. Gatesy, J., et al. 2013. A phylogenetic blueprint for a modern whale. Molecular Phylogenet- ics and Evolution 66 (2):479–506. doi:10.1016/j.ympev.2012.10.012. Mayr, E. 2001. What Evolution Is. New York: Basic Books. Uhen, M. 2010. The Origin(s) of Whales. Annual Review of Earth and Planetary Sciences 38:189–219. University of California Museum of Paleontology. 2011. Misconceptions about evolution and the mechanisms of evolution. Understanding Evolution. http://evolution. berke- ley.edu/evolibrary/misconceptions_faq. php. Zimmer, C. 1998. At the Water’s Edge: Macroevolution and the Transformation of Life. New York: Free Press.

Cited Literature Connor, R. C. 2007. Dolphin Social Intelligence: Complex Alliance Relationships in Bottlenose Dolphins and a Consideration of Selective Environments for Extreme Brain Size Evolution in Mammals. Philosophical Transactions of the Royal Society B: Biological Sciences 362 (1480):587– 602. doi:10.1098/rstb.2006.1997. Cooper, L. N., J. G. M. Thewissen, and S. T. Hussain. 2009. New Early–Middle Eocene Archaeocetes (Pakicetidae and Remingtonocetidae, Cetacea) from the Kuldana Formation of Northern Pakistan. Journal of Vertebrate Paleontology 29: 1289–99. Dobzhansky, T. 1973. Nothing in Biology Makes Sense Except in the Light of Evolution. American Biology Teacher 35:125–29. Gingerich, P. D., K. D. Rose, and D. W. Krause. 1980. Early Cenozoic Mammalian Faunas of the Clark’s Fork Basin–Polecat Bench Area, Northwestern Wyoming. University of Michigan Papers on Paleontology 24:51–68. Gingerich, P. D., N. A. Wells, D. E. Russell, and S. M. I. Shah. 1983. Origin of Whales in Epicontinental Remnant Seas: New Evidence from the Early Eocene of Pakistan. Science 220:403–6. doi:10.1126/science.220.4595.403. Luo, Z., and P. D. Gingerich. 1999. Terrestrial Mesonychia to Aquatic Cetacea: Trans- formation of the Basicranium and Evolution of Hearing in Whales. University of Michigan Papers on Paleontology 31:1–98. Marino, L. 2007. Cetacean Brains: How Aquatic Are They? Anatomical Record 290 (6):694– 700. doi:10.1002/ar.20530. Marx, F. G., and M. D. Uhen. 2010. Climate, Critters, and Cetaceans: Cenozoic Drivers of the Evolution of Modern Whales. Science 327:993–96. doi:10.1126/science.1185581. Nummela, S., S. T. Hussain, and J. G. M. Thewissen. 2006. Cranial Anatomy of Pakideti- dae (Cetacea, Mammalia). Journal of Vertebrate Paleontology 26 (3):746–59. Stable URL: http://www.jstor.org/stable/4524618. Price, S. A., O. R. P. Bininda-Emonds, and J. L. Gittleman. 2005. A Complete Phylogeny of the Whales, Dolphins and Even-Toed Hoofed Mammals (Cetartiodactyla). Biological Reviews 80 (3):445–73. doi:10.1017/s1464793105006743. Thewissen, J. G. M., M. J. Cohn, L. S. Stevens, S. Bajpai, J. Heyning, et al. 2006. Developmental Basis for Hind-Limb Loss in Dolphins and Origin of the Cetacean Bodyplan. Proceedings of the National Academy of Science 103:8414–18. doi:10.1073/ pnas.0602920103. Thewissen, J., L. Cooper, J. George, and S. Bajpai. 2009. From Land to Water: The Origin of Whales, Dolphins, and Porpoises. Evolution: Education and Outreach 2 (2):272–88. doi:10.1007/s12052-009-0135-2.

18 CHAPTER 1 | WALKING WHALES © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES Thewissen,NOT J. G. M., S. I. Madar, E. Ganz, FOR S. T. Hussain, M. Arif, et al. 1997.SALE Fossil Yak (Bos Grunniens: Artiodactyla, Mammalia) from the Himalayas of Pakistan. Kirt- landia (Cleveland) 50:11–16. Turvey, S. T. 2009. Witness to Extinction: How We Failed to Save the Yangtze River Dolphin. Oxford: Oxford University Press. Uhen, M. 2010. The Origin(s) of Whales. Annual Review of Earth and Planetary Sciences 38:189–219. doi:10.1146/annurev-earth-040809-152453. Zimmer, C. 1998. At the Water’s Edge: Macroevolution and the Transformation of Life. New York: Free Press.

CITED LITERATURE 19 © Roberts and Company Publishers, ISBN: 9781936221448, due August 23, 2013, For examination purposes only FINAL PAGES