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34 The Origin and Evolution of Vertebrates Figure 34.1 What is the relationship of this ancient organism to humans? KEY CONCEPTS 34.1 Chordates have a notochord and a dorsal, hollow nerve cord Craniates are chordates that have a head Vertebrates are craniates that have a backbone Gnathostomes are vertebrates that have jaws Tetrapods are gnathostomes that have limbs Amniotes are tetrapods that have a terrestrially adapted egg 34.7 Mammals are amniotes that have hair and produce milk 34.8 Humans are mammals that have a large brain and bipedal locomotion 34.2 34.3 34.4 34.5 34.6 OVERVIEW Half a Billion Years of Backbones E arly in the Cambrian period, some 530 million years ago, an immense variety of invertebrate animals inhabited Earth’s oceans. Predators used sharp claws and mandibles to skewer their prey. Many animals had protective spikes or armor as well as modiﬁed mouthparts that enabled their bearers to ﬁlter food from the water. Worms slithered in the bottom muck, feeding on organic matter. Amidst this bustle, it would have been easy to overlook certain slender, 3-cm-long creatures gliding through the water: Myllokunmingia fengjiaoa (Figure 34.1). Although lacking armor and appendages, this ancient species was closely related to one of the most successful groups of animals ever to swim, walk, slither, or ﬂy: the vertebrates, which derive their name from vertebrae, the series of bones that make up the vertebral column, or backbone. For more than 150 million years, vertebrates were restricted to the oceans, but about 365 million years ago, the evolution of limbs in one lineage of vertebrates set the stage for these vertebrates to colonize land. There they diversiﬁed into amphibians, reptiles (including birds), and mammals. There are approximately 52,000 species of vertebrates, a relatively small number compared to, say, the 1 million insect species on Earth. But what vertebrates lack in species diversity they make up for in disparity, varying enormously in characteristics such as body mass. Vertebrates include the heaviest animals ever to walk on land, plant-eating dinosaurs as massive as 40,000 kg (more than 13 pickup trucks). They also include the biggest animal ever to exist on Earth, the blue whale, which can exceed a mass of 100,000 kg. On the other end of the spectrum, a ﬁsh discovered in 2004 is just 8.4 mm long and has a mass roughly 100 billion times smaller than that of a blue whale. In this chapter, you will learn about current hypotheses regarding the origins of vertebrates from invertebrate ancestors. We will track the evolution of the vertebrate body plan, from a notochord to a head to a mineralized skeleton. We’ll also explore the major groups of vertebrates (both living and extinct), as well as the evolutionary history of our own species. CONCEPT 34.1 Chordates have a notochord and a dorsal, hollow nerve cord Vertebrates are members of the phylum Chordata, the chordates. Chordates are bilaterian (bilaterally symmetrical) animals, and within Bilateria, they belong to the clade of animals known as Deuterostomia (see Chapter 32). The bestknown deuterostomes, aside from vertebrates, are the echinoderms, the group that includes sea stars and sea urchins. CHAPTER 34 The Origin and Evolution of Vertebrates 697 Echinodermata (sister group to chordates) Urochordata (tunicates) Common ancestor of chordates Myxini (hagfishes) Dipnoi (lungfishes) Lobed fins Reptilia (turtles, snakes, crocodiles, birds) Limbs with digits Amniotic egg However, as shown in Figure 34.2, the cephalochordates and the urochordates are two groups of invertebrate deuterostomes that are more closely related to vertebrates than to other invertebrates. Along with the hagﬁshes and the vertebrates, they make up the chordates. Milk Mammalia (mammals) Tetrapods Amphibia (frogs, salamanders) Amniotes Figure 34.2 Phylogeny of living chordates. This phylogenetic hypothesis shows the major clades of chordates in relation to the other main deuterostome clade, Echinodermata (see Chapter 33). For selected clades, some of the derived characters are listed; for example, all chordates, and only chordates, have a notochord. Lobe-fins Actinistia (coelacanths) Lungs or lung derivatives Osteichthyans Actinopterygii (ray-finned fishes) Jaws, mineralized skeleton Gnathostomes Chondrichthyes (sharks, rays, chimaeras) Vertebral column Vertebrates Petromyzontida (lampreys) Head Craniates Notochord Chordates Cephalochordata (lancelets) ANCESTRAL DEUTEROSTOME Dorsal, hollow nerve cord Muscle segments Notochord Derived Characters of Chordates All chordates share a set of derived characters, though many species possess some of these traits only during embryonic development. Figure 34.3 illustrates four key characters of chordates: a notochord; a dorsal, hollow nerve cord; pharyngeal slits or clefts; and a muscular, post-anal tail. Mouth Anus Muscular, post-anal tail Pharyngeal slits or clefts Notochord Figure 34.3 Chordate characteristics. All chordates possess the four highlighted structural trademarks at some point during their development. Chordates are named for a skeletal structure, the notochord, present in all chordate embryos as well as in some adult chordates. The notochord is a longitudinal, ﬂexible rod located between the digestive tube and the nerve cord. It is composed of large, ﬂuid-ﬁlled cells encased in fairly stiff, ﬁbrous tissue. The notochord provides skeletal support throughout most of the length of a chordate, and in larvae or adults that retain it, it also provides a ﬁrm but ﬂexible structure against which muscles can work during swimming. In most vertebrates, a more complex, jointed skeleton develops around the ancestral notochord, and the adult retains only remnants of the embryonic 698 UNIT FIVE The Evolutionary History of Biological Diversity notochord. In humans, the notochord is reduced and forms part of the gelatinous disks sandwiched between the vertebrae. Dorsal, Hollow Nerve Cord The nerve cord of a chordate embryo develops from a plate of ectoderm that rolls into a tube located dorsal to the notochord. The resulting dorsal, hollow nerve cord is unique to chordates. Other animal phyla have solid nerve cords, and in most cases they are ventrally located. The nerve cord of a chordate embryo develops into the central nervous system: the brain and spinal cord. Pharyngeal Slits or Clefts The digestive tube of chordates extends from the mouth to the anus. The region just posterior to the mouth is the pharynx. In all chordate embryos, a series of pouches separated by grooves forms along the sides of the pharynx. In most chordates, these grooves (known as pharyngeal clefts) develop into slits that open to the outside of the body. These pharyngeal slits allow water entering the mouth to exit the body without passing through the entire digestive tract. Pharyngeal slits function as suspension-feeding devices in many invertebrate chordates. In vertebrates (with the exception of vertebrates with limbs, the tetrapods), these slits and the structures that support them have been modiﬁed for gas exchange and are known as gill slits. In tetrapods, the pharyngeal clefts do not develop into slits. Instead, they play an important role in the development of parts of the ear and other structures in the head and neck. Muscular, Post-Anal Tail Chordates have a tail that extends posterior to the anus, although in many species it is greatly reduced during embryonic development. In contrast, most nonchordates have a digestive tract that extends nearly the whole length of the body. The chordate tail contains skeletal elements and muscles, and it helps propel many aquatic species in the water. Lancelets The most basal (earliestdiverging) group of living chordates are animals called lancelets (Cephalochordata), which get their name from their bladelike shape (Figure 34.4). As larvae, lancelets develop a notochord, a dorsal, hollow nerve cord, numerous pharyngeal slits, and a post-anal tail. The larvae feed on plankton in the water column, alternating between upward swimming and passive sinking. As the larvae sink, they trap plankton and other suspended particles in their pharynx. Adult lancelets can reach 6 cm in length. They retain key chordate traits, closely resembling the idealized chordate shown in Figure 34.3. Following metamorphosis, an adult lancelet swims down to the seaﬂoor and wriggles backward into the sand, leaving only its anterior end exposed. Cilia draw seawater into the lancelet’s mouth. A net of mucus secreted across the pharyngeal slits removes tiny food particles as the water passes through the slits, and the trapped food enters the intestine. The pharynx and pharyngeal slits play a minor role in gas exchange, which occurs mainly across the external body surface. A lancelet frequently leaves its burrow to swim to a new location. Though feeble swimmers, these invertebrate chordates display, in a simple form, the swimming mechanism of ﬁshes. Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia Cirri Mouth Pharyngeal slits Atrium Notochord Digestive tract 1 cm Atriopore Dorsal, hollow nerve cord Segmental muscles Anus Tail Figure 34.4 The lancelet Branchiostoma, a cephalochordate. This small invertebrate displays all four main chordate characters. Water enters the mouth and passes through the pharyngeal slits into the atrium, a chamber that vents to the outside via the atriopore; large particles are blocked from entering the mouth by tentacle-like cirri. The serially arranged segmental muscles produce the lancelet’s wavelike swimming movements. CHAPTER 34 The Origin and Evolution of Vertebrates 699 Coordinated contraction of muscles arranged like rows of chevrons (⬍⬍⬍⬍) along the sides of the notochord ﬂexes the notochord, producing side-to-side undulations that thrust the body forward. This serial arrangement of muscles is evidence of the lancelet’s segmentation. The muscle segments develop from blocks of mesoderm called somites, which are found along each side of the notochord in all chordate embryos. Globally, lancelets are rare, but in a few regions (including Tampa Bay, along the Florida coast), they occasionally reach densities in excess of 5,000 individuals per square meter. Tunicates Contrary to what was formerly thought, recent molecular studies suggest that the tunicates (Urochordata) are more closely related to other chordates than are lancelets. The chordate characters of tunicates are most apparent during their larval stage, which may be as brief as a few minutes (Figure 34.5a). In many species, the larva uses its tail muscles and notochord to swim through water in search of a suitable substrate on which it can settle, guided by cues it receives from light- and gravity-sensitive cells. Once a tunicate has settled on a substrate, it undergoes a radical metamorphosis in which many of its chordate characters disappear. Its tail and notochord are resorbed; its nervous system degenerates; and its remaining organs rotate 90°. As an adult, a tunicate draws in water through an incurrent siphon; Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia the water then passes through the pharyngeal slits into a chamber called the atrium and exits through an excurrent siphon (Figure 34.5b and c). Food particles are ﬁltered from the water by a mucous net and transported by cilia to the esophagus. The anus empties into the excurrent siphon. Some tunicate species shoot a jet of water through their excurrent siphon when attacked, earning them the informal name of “sea squirts.” The loss of chordate characters in the adult stage of tunicates appears to have occurred after the tunicate lineage branched off from other chordates. Even the tunicate larva appears to be highly derived. For example, tunicates have 9 Hox genes, whereas all other chordates studied to date—including the early-diverging lancelets—share a set of 13 Hox genes. The apparent loss of 4 Hox genes indicates that the chordate body plan of a tunicate larva is built using a different set of genetic controls than other chordates. Early Chordate Evolution Although lancelets and tunicates are relatively obscure animals, they occupy key positions in the history of life and can provide clues about the evolutionary origin of vertebrates. As you have read, for example, lancelets display key chordate characters as adults, and their lineage branches from the base of the chordate phylogenetic tree. These ﬁndings suggest that the ancestral chordate may have looked something like a lancelet—that is, it had an anterior end with a mouth; a notochord; a dorsal, hollow nerved cord; pharyngeal slits; and a post-anal tail. Research on lancelets has also revealed important clues about the evolution of the chordate brain. Rather than a fullﬂedged brain, lancelets have only a slightly swollen tip on the anterior end of their dorsal nerve cord. But the same Hox genes that organize major regions of the forebrain, midbrain, Water flow Notochord Incurrent siphon to mouth Excurrent siphon Dorsal, hollow nerve cord Tail Excurrent siphon Muscle segments Excurrent siphon Incurrent siphon Anus Pharynx with numerous slits Intestine Tunic Intestine Stomach Atrium Esophagus Pharynx with slits (a) A tunicate larva is a free-swimming but nonfeeding “tadpole” in which all four main characters of chordates are evident. Stomach (b) In the adult, prominent pharyngeal slits function in suspension feeding, but other chordate characters are not obvious. Figure 34.5 A tunicate, a urochordate. 700 UNIT FIVE Atrium The Evolutionary History of Biological Diversity (c) An adult tunicate, or sea squirt, is a sessile animal (photo is approximately life-sized). BF1 Otx Hox3 Nerve cord of lancelet embryo BF1 Otx Hox3 Brain of vertebrate embryo (shown straightened) Forebrain Midbrain Hindbrain Figure 34.6 Expression of developmental genes in lancelets and vertebrates. Hox genes (including BF1, Otx, and Hox3) control the development of major regions of the vertebrate brain. These genes are expressed in the same anterior-to-posterior order in lancelets and vertebrates. Each colored bar is positioned above the portion of the brain whose development that gene controls. MAKE CONNECTIONS What do these results and those in Figure 21.18 indicate about Hox genes and their evolution? and hindbrain of vertebrates express themselves in a corresponding pattern in this small cluster of cells in the lancelet’s nerve cord (Figure 34.6). This suggests that the vertebrate brain is an elaboration of an ancestral structure similar to the lancelet’s simple nerve cord tip. As for tunicates, their genome has been completely sequenced and can be used to identify genes likely to have been present in early chordates. Researchers taking this approach have suggested that ancestral chordates had genes associated with vertebrate organs such as the heart and thyroid gland. These genes are found in tunicates and vertebrates but are absent from nonchordate invertebrates. In contrast, tunicates lack many genes that in vertebrates are associated with the long-range transmission of nerve impulses. This result suggests that such genes arose in an early vertebrate and are unique to the vertebrate evolutionary lineage. CONCEPT CHECK chordate evolution was the appearance of a head. Chordates with a head are known as craniates (from the word cranium, skull). The origin of a head—consisting of a brain at the anterior end of the dorsal nerve cord, eyes and other sensory organs, and a skull—enabled chordates to coordinate more complex movement and feeding behaviors. (Note that heads evolved independently in other animal lineages as well; see Chapter 33.) Derived Characters of Craniates Living craniates share a set of derived characters that distinguish them from other chordates. As a result of gene duplication, craniates possess two or more sets of Hox genes (lancelets and tunicates have only one). Other important families of genes that produce signaling molecules and transcription factors are also duplicated in craniates. Divergence of sequences in the duplicate genes led to additional genetic complexity. This may have made it possible for craniates to develop more complex morphologies than those of lancelets and tunicates. One feature unique to craniates is the neural crest, a collection of cells that appears near the dorsal margins of the closing neural tube in an embryo (Figure 34.7). Neural crest cells disperse throughout the body, where they give rise to a variety of structures, including teeth, some of the bones and cartilage of the skull, the inner layer of skin (dermis) of the facial region, several types of neurons, and the sensory capsules in which eyes and other sense organs develop. In aquatic craniates, the pharyngeal clefts evolved into gill slits. Unlike the pharyngeal slits of lancelets, which are used primarily for suspension feeding, gill slits are associated with muscles and nerves that allow water to be pumped through Dorsal edges of neural plate Neural crest Neural tube 34.1 1. Identify four derived characters that all chordates have at some point during their life. 2. You are a chordate, yet you lack most of the main derived characters of chordates. Explain. 3. WHAT IF? Suppose lancelets lacked a gene found in tunicates and vertebrates. Would this imply that the chordates’ most recent common ancestor also lacked this gene? Explain. For suggested answers, see Appendix A. 34.2 Notochord Migrating neural crest cells (b) Neural crest cells migrate to (a) The neural crest consists of distant sites in the embryo. bilateral bands of cells near the margins of the embryonic folds that form the neural tube. Craniates are chordates that have a head (c) The migrating neural crest cells give rise to some of the anatomical structures unique to vertebrates, including some of the bones and cartilage of the skull. (A fetal human skull is depicted here.) After the evolution of the basic chordate body plan, that seen in lancelets and tunicate larvae, the next major transition in Figure 34.7 The neural crest, embryonic source of many unique craniate characters. CONCEPT CHAPTER 34 The Origin and Evolution of Vertebrates 701 the slits. This pumping can assist in sucking in food, and it facilitates gas exchange. (In terrestrial craniates, the pharyngeal clefts develop into other structures, as we’ll explain later.) Craniates, which are more active than lancelets and tunicates, also have a higher metabolic rate and a much more extensive muscular system. Muscles lining their digestive tract aid digestion by moving food through the tract. Craniates also have a heart with at least two chambers, red blood cells with hemoglobin, and kidneys that remove waste products from the blood. The Origin of Craniates In the late 1990s, paleontologists working in China discovered a vast supply of fossils of early chordates that appear to straddle the transition to craniates. The fossils were formed during the Cambrian explosion 530 million years ago, when many groups of animals were diversifying (see Chapter 32). The most primitive of the fossils are the 3-cm-long Haikouella (Figure 34.8). In many ways, Haikouella resembled a lancelet. Its mouth structure indicates that, like lancelets, it probably was a suspension feeder. However, Haikouella also had some of the characters of craniates. For example, it had a well-formed brain, small eyes, and muscle segments along the body, as do the vertebrate ﬁshes. It also had respiratory gills in its pharynx, which all the more basal chordates lack. However, Haikouella did not have a skull or ear organs, suggesting that these characters emerged with further innovations to the chordate nervous system. (The earliest “ears” were organs for maintaining balance, a function still performed by the ears of humans and other living vertebrates.) In other Cambrian rocks, paleontologists have found fossils of more advanced chordates, such as Myllokunmingia (see Figure 34.1). About the same size as Haikouella, Myllokunmingia had ear capsules and eye capsules, parts of the skull that surround these organs. Based on these and other characters, paleontologists have identiﬁed Myllokunmingia as a true craniate. Hagﬁshes The most basal group of craniates is Myxini, the hagﬁshes (Figure 34.9). Hagﬁshes have a skull made of cartilage, but they lack jaws and vertebrae. They swim in a snakelike fashion by using their segmental muscles to exert force against their notochord, which they retain in adulthood as a strong, ﬂexible rod of cartilage. Hagﬁshes have a small brain, eyes, ears, and a nasal opening that connects with the pharynx. Their mouths contain toothlike formations made of the protein keratin. All of the 30 living species of hagﬁshes are marine. Measuring up to 60 cm in length, most are bottom-dwelling scavengers that feed on worms and sick or dead ﬁsh. Rows of slime glands on a hagﬁsh’s ﬂanks secrete a substance that absorbs water, forming a slime that may repulse other scavengers when a hagﬁsh is feeding (see Figure 34.9). When attacked by a predator, a hagﬁsh can produce several liters of slime in less than a minute. The slime coats the gills of the attacking ﬁsh, sending it into retreat or even suffocating it. Several teams of biologists and engineers are investigating the properties of hagﬁsh slime in hopes of producing an artiﬁcial slime that could act as a space-ﬁlling gel. Such a gel might be used, for instance, to curtail bleeding during surgery. Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia Slime glands 5 mm Segmented muscles Pharyngeal slits Figure 34.8 Fossil of an early chordate. Discovered in 1999 in southern China, Haikouella had eyes and a brain but lacked a skull, a derived trait of craniates. The colors in the illustration are fanciful. 702 UNIT FIVE The Evolutionary History of Biological Diversity Figure 34.9 A hagﬁsh. CONCEPT CHECK 34.2 1. What characteristics do hagﬁshes have that lancelets and tunicates lack? 2. Which extinct chordate is more closely related to humans, Myllokunmingia or Haikouella? Explain. 3. WHAT IF? In several different animal lineages, organisms with a head ﬁrst appeared roughly 530 million years ago. Does this ﬁnding constitute proof that having a head is favored by natural selection? Explain. For suggested answers, see Appendix A. CONCEPT Figure 34.10 A sea lamprey. Most lampreys use their mouth (inset) and tongue to bore a hole in the side of a ﬁsh. The lamprey then ingests the blood and other tissues of its host. 34.3 Vertebrates are craniates that have a backbone During the Cambrian period, a lineage of craniates gave rise to vertebrates. With a more complex nervous system and a more elaborate skeleton than those of their ancestors, vertebrates became more efﬁcient at two essential tasks: capturing food and avoiding being eaten. Derived Characters of Vertebrates After vertebrates branched off from other craniates, they underwent another gene duplication, this one involving a group of transcription factor genes called the Dlx family. The resulting additional genetic complexity may be associated with innovations in the vertebrate nervous system and skeleton, including a more extensive skull and a backbone composed of vertebrae. In some vertebrates, the vertebrae are little more than small prongs of cartilage arrayed dorsally along the notochord. In the majority of vertebrates, however, the vertebrae enclose the spinal cord and have taken over the mechanical roles of the notochord. Aquatic vertebrates also acquired dorsal, ventral, and anal ﬁns stiffened by bony structures called ﬁn rays, which provide thrust and steering control when swimming after prey or away from predators. Faster swimming was supported by other adaptations, including a more efﬁcient gas exchange system in the gills. Lampreys Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia Lampreys (Petromyzontida) are the most basal lineage of living vertebrates. Like hagﬁshes, lampreys may offer clues to early chordate evolution, but they have also acquired unique characters. There are about 35 species of lampreys inhabiting various marine and freshwater environments (Figure 34.10). Most are parasites that feed by clamping their round, jawless mouth onto the ﬂank of a live ﬁsh. They then use their rasping tongue to penetrate the skin of the ﬁsh and ingest the ﬁsh’s blood. As larvae, lampreys live in freshwater streams. The larva is a suspension feeder that resembles a lancelet and spends much of its time partially buried in sediment. Some species of lampreys feed only as larvae; following several years in streams, they mature sexually, reproduce, and die within a few days. Most lampreys, however, migrate to the sea or lakes as they mature into adults. Sea lampreys (Petromyzon marinus) have invaded the Great Lakes over the past 170 years and have devastated a number of ﬁsheries there. The skeleton of lampreys is made of cartilage. Unlike the cartilage found in most vertebrates, lamprey cartilage contains no collagen. Instead, it is a stiff matrix of other proteins. The notochord of lampreys persists as the main axial skeleton in the adult, as it does in hagﬁshes. However, lampreys also have a ﬂexible sheath around their rodlike notochord. Along the length of this sheath, pairs of cartilaginous projections related to vertebrae extend dorsally, partially enclosing the nerve cord. Fossils of Early Vertebrates After the ancestors of lampreys branched off from other vertebrates during the Cambrian period, many other lineages of vertebrates emerged. Like lampreys, the early members of these lineages lacked jaws, but the resemblance stopped there. Conodonts were slender, soft-bodied vertebrates with prominent eyes controlled by numerous muscles. Most conodonts were 3–10 cm in length, although some may have been as long as 30 cm. They probably hunted with the help of their large eyes, impaling prey on a set of barbed hooks at the anterior end of their mouth. These hooks were made of dental tissues that were mineralized—composed of minerals such as calcium that provide rigidity (Figure 34.11). The food was then passed back to the pharynx, where a different set of dental elements sliced and crushed the food. CHAPTER 34 The Origin and Evolution of Vertebrates 703 jawless, armored swimming vertebrates, but they all became extinct by the end of the Devonian period. Origins of Bone and Teeth Dental elements (within head) Figure 34.11 A conodont. Conodonts were early vertebrates that lived from the late Cambrian until the late Triassic. Unlike lampreys, conodonts had mineralized mouthparts, which they used for either predation or scavenging. Conodonts were extremely abundant for over 300 million years. Their fossilized dental elements are so plentiful that they have been used for decades by petroleum geologists as guides to the age of rock layers in which they search for oil. (These elements also gave conodonts their name, which means “cone teeth.”) Vertebrates with additional innovations emerged during the Ordovician, Silurian, and Devonian periods. These vertebrates had paired ﬁns and, as in lampreys, an inner ear with two semicircular canals that provided a sense of balance. Although they, too, lacked jaws, they had a muscular pharynx, which they may have used to suck in bottom-dwelling organisms or detritus. They were also armored with mineralized bone, which covered varying amounts of their body (Figure 34.12). The armor, which in some species included spines, may have offered protection from predators. There were many species of these The human skeleton is heavily mineralized bone, whereas cartilage plays a fairly minor role. But a bony skeleton was a relatively late development in the history of vertebrates. As we’ve seen, the vertebrate skeleton evolved initially as a structure made of unmineralized cartilage. What initiated the process of mineralization in vertebrates? One hypothesis is that mineralization was associated with a transition in feeding mechanisms. Early chordates probably were suspension feeders, like lancelets, but over time they became larger and were able to ingest larger particles, including some small animals. The earliest known mineralized structures in vertebrates—conodont dental elements—were an adaptation that may have allowed these animals to become scavengers and predators. In addition, when the bony armor of later jawless vertebrates was examined under the microscope, scientists found that it was composed of small tooth-like structures. These ﬁndings suggest that mineralization of the vertebrate body may have begun in the mouth and later was incorporated into protective armor. Only in more derived vertebrates did the endoskeleton begin to mineralize, starting with the skull. As you’ll read in the next section, more recent lineages of vertebrates underwent even further mineralization. CONCEPT CHECK 34.3 1. How are differences in the anatomy of lampreys and conodonts reﬂected in each animal’s feeding method? 2. WHAT IF? Suggest key roles that mineralized bone might have played in early vertebrates. For suggested answers, see Appendix A. CONCEPT 34.4 Gnathostomes are vertebrates that have jaws Hagﬁshes and lampreys are survivors from the early Paleozoic era, when jawless craniates were common. Since then, jawless vertebrates have been far outnumbered by jawed vertebrates, known as gnathostomes. Living gnathostomes are a diverse group that includes sharks and their relatives, rayﬁnned ﬁshes, lobe-ﬁnned ﬁshes, amphibians, reptiles (including birds), and mammals. Pteraspis Pharyngolepis Figure 34.12 Jawless armored vertebrates. Pteraspis and Pharyngolepis were two of many genera of jawless vertebrates that emerged during the Ordovician, Silurian, and Devonian periods. 704 UNIT FIVE The Evolutionary History of Biological Diversity Derived Characters of Gnathostomes Gnathostomes (“jaw mouth”) are named for their jaws, hinged structures that, especially with the help of teeth, enable gnathostomes to grip food items ﬁrmly and slice them. Figure 34.13 Hypothesis for the evolution of vertebrate jaws. The skeleton of the jaws and their supports may have evolved from two pairs of skeletal rods (red and green) located between gill slits near the mouth. According to this hypothesis, pairs of rods anterior to those that formed the jaws were either lost or incorporated into the cranium or jaws. Gill slits 0.5 m Cranium Mouth Skeletal rods Figure 34.14 Fossil of an early gnathostome. The placoderm Dunkleosteus grew up to 10 m in length. A 2006 analysis of its jaw structure concluded that Dunkleosteus could exert a force of 560 kg/cm2 (8,000 pounds per square inch) at the tip of its jaws. According to one hypothesis, gnathostome jaws evolved by modiﬁcation of the skeletal rods that had previously supported the anterior pharyngeal (gill) slits (Figure 34.13). The remaining gill slits, no longer required for suspension feeding, remained as the major sites of respiratory gas exchange with the external environment. Gnathostomes share other derived characters besides jaws. The common ancestors of all gnathostomes underwent an additional duplication of Hox genes, such that the single set present in early chordates became four. In fact, the entire genome appears to have duplicated, and together these genetic changes likely enabled the origin of jaws and other novel features in gnathostomes. The gnathostome forebrain is enlarged compared to that of other craniates, mainly in association with enhanced senses of smell and vision. Another characteristic of aquatic gnathostomes is the lateral line system, organs that form a row along each side of the body and are sensitive to vibrations in the surrounding water. Precursors of these organs were present in the head shields of some jawless vertebrates. Fossil Gnathostomes Gnathostomes appeared in the fossil record in the late Ordovician period, about 450 million years ago, and steadily became more diverse. Their success probably resulted from a combination of anatomical features: Their paired ﬁns and tail (which were also found in jawless vertebrates) allowed them to swim efﬁciently after prey, and their jaws enabled them to grab prey or simply bite off chunks of ﬂesh. The earliest gnathostomes in the fossil record include extinct lineages of armored vertebrates known as placoderms, which means “plate-skinned.” Most placoderms were less than a meter long, though some giants measured more than 10 m (Figure 34.14). Other groups of jawed vertebrates, collectively called acanthodians, emerged at roughly the same time and radiated during the Silurian and Devonian periods (444–359 million years ago). Placoderms had disappeared by 359 million years ago, and acanthodians became extinct about 70 million years later. In the past several years, new fossil discoveries have revealed that 450–420 million years ago was a period of tumultuous evolutionary change. Gnathostomes that lived during this period had highly variable forms, and by 420 million years ago, they had diverged into the three lineages of jawed vertebrates that survive today: chondrichthyans, ray-ﬁnned ﬁshes, and lobe-ﬁns. Chondrichthyans (Sharks, Rays, and Their Relatives) Sharks, rays, and their relatives include some of the biggest and most successful vertebrate predators in the oceans. They belong to the clade Chondrichthyes, which means “cartilage ﬁsh.” As their name indicates, the chondrichthyans have a skeleton composed predominantly of cartilage, though often impregnated with calcium. When the name Chondrichthyes was ﬁrst coined in the 1800s, scientists thought that chondrichthyans represented an early stage in the evolution of the vertebrate skeleton and that mineralization had evolved only in more derived lineages (such Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia CHAPTER 34 The Origin and Evolution of Vertebrates 705 as “bony ﬁshes”). However, as conodonts and armored jawless vertebrates demonstrate, the mineralization of the vertebrate skeleton had already begun before the chondrichthyan lineage branched off from other vertebrates. Moreover, bone-like tissues have been found in early chondrichthyans, such as the ﬁn skeleton of a shark that lived in the Carboniferous period. Traces of bone can also be found in living chondrichthyans—in their scales, at the base of their teeth, and, in some sharks, in a thin layer on the surface of their vertebrae. Such ﬁndings strongly suggest that the restricted distribution of bone in the chondrichthyan body is a derived condition, emerging after chondrichthyans diverged from other gnathostomes. There are about 1,000 species of living chondrichthyans. The largest and most diverse group consists of the sharks, rays, and skates (Figure 34.15a and b). A second group is composed of a few dozen species of ratﬁshes, or chimaeras (Figure 34.15c). Most sharks have a streamlined body and are swift swimmers, but they do not maneuver very well. Powerful movements of the trunk and the tail ﬁn propel them forward. The dorsal ﬁns function mainly as stabilizers, and the paired pectoral (fore) and pelvic (hind) ﬁns are important for maneuvering. Although a shark gains buoyancy by storing a large amount of oil in its huge liver, the animal is still more dense than water, and if it stops swimming it sinks. Continual swimming also ensures that water ﬂows into the shark’s mouth and out through the gills, where gas exchange occurs. However, some sharks and many skates and rays spend a good deal of time resting on the seaﬂoor. When resting, they use muscles of their jaws and pharynx to pump water over the gills. The largest sharks and rays are suspension feeders that consume plankton. Most sharks, however, are carnivores that swallow their prey whole or use their powerful jaws and sharp teeth to tear ﬂesh from animals too large to swallow in one piece. Sharks have several rows of teeth that gradually move to the front of the mouth as old teeth are lost. The digestive tract of many sharks is proportionately shorter than that of many other vertebrates. Within the shark intestine is a spiral valve, a corkscrew-shaped ridge that increases surface area and prolongs the passage of food through the digestive tract. Acute senses are adaptations that go along with the active, carnivorous lifestyle of sharks. Sharks have sharp vision but cannot distinguish colors. The nostrils of sharks, like those of most aquatic vertebrates, open into dead-end cups. They function only for olfaction (smelling), not for breathing. Like some other vertebrates, sharks have a pair of regions in the skin of their head that can detect electric ﬁelds generated by the muscle contractions of nearby animals. Like all (nonmammalian) aquatic vertebrates, sharks have no eardrums, structures that terrestrial vertebrates use to transmit sound waves in air to the auditory organs. Sound reaches a shark through water, and the animal’s entire body transmits the sound to the hearing organs of the inner ear. 706 UNIT FIVE The Evolutionary History of Biological Diversity Dorsal fins Pectoral fins Pelvic fins (a) Blacktip reef shark (Carcharhinus melanopterus). Sharks are fast swimmers with acute senses. Like all gnathosomes, they have paired pectoral and pelvic fins. (b) Southern stingray (Dasyatis americana). Most rays are bottomdwellers that feed on molluscs and crustaceans. Some rays cruise in open water and scoop food into their gaping mouth. (c) Spotted ratfish (Hydrolagus colliei). Ratfishes, or chimaeras, typically live at depths greater than 80 m and feed on shrimp, molluscs, and sea urchins. Some species have a venomous spine at the front of their first dorsal fin. Figure 34.15 Chondrichthyans. Shark eggs are fertilized internally. The male has a pair of claspers on its pelvic ﬁns that transfer sperm into the reproductive tract of the female. Some species of sharks are oviparous; they lay eggs that hatch outside the mother’s body. These sharks release their eggs after encasing them in protective coats. Other species are ovoviviparous; they retain the fertilized eggs in the oviduct. Nourished by the egg yolk, the embryos develop into young that are born after hatching within the uterus. A few species are viviparous; the young develop within the uterus and obtain nourishment prior to birth by receiving nutrients from the mother’s blood through a yolk sac placenta, by absorbing a nutritious ﬂuid produced by the uterus, or by eating other eggs. The reproductive tract of the shark empties along with the excretory system and digestive tract into the cloaca, a common chamber that has a single opening to the outside. Although rays are closely related to sharks, they have adopted a very different lifestyle. Most rays are bottomdwellers that feed by using their jaws to crush molluscs and crustaceans. They have a ﬂattened shape and use their greatly enlarged pectoral ﬁns like water wings to propel themselves through the water. The tail of many rays is whiplike and, in some species, bears venomous barbs that function in defense. Chondrichthyans have thrived for over 400 million years. Today, however, they are severely threatened with overﬁshing. A recent report indicated that shark stocks in the northwest Atlantic had declined 75% over a 15-year period. Ray-Finned Fishes and Lobe-Fins Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia The vast majority of vertebrates belong to the clade of gnathostomes called Osteichthyes. Unlike chondrichthyans, nearly all living osteichthyans have an ossiﬁed (bony) endoskeleton with a hard matrix of Spinal cord calcium phosphate. Like many other taxonomic names, the name Osteichthyes (“bony ﬁsh”) was coined long before the advent of phylogenetic systematics. When it was originally deﬁned, the group excluded tetrapods, but we now know that such a taxon would be paraphyletic (see Figure 34.2). Therefore, systematists today include tetrapods along with bony ﬁshes in the clade Osteichthyes. Clearly, the name of the group does not accurately describe all of its members. In this section, we’ll discuss the aquatic osteichthyans known informally as ﬁshes. Most ﬁshes breathe by drawing water over four or ﬁve pairs of gills located in chambers covered by a protective bony ﬂap called the operculum (Figure 34.16). Water is drawn into the mouth, through the pharynx, and out between the gills by movement of the operculum and contraction of muscles surrounding the gill chambers. Most ﬁshes can control their buoyancy with an air sac known as a swim bladder. Movement of gases from the blood to the swim bladder increases buoyancy, making the animal rise; transfer of gas back to the blood causes the animal to sink. Charles Darwin proposed that the lungs of tetrapods evolved from swim bladders, but strange as it may sound, the opposite seems to be true. Osteichthyans in many earlybranching lineages have lungs, which they use to breathe air as a supplement to gas exchange in their gills. The weight of evidence indicates that lungs arose in early osteichthyans; later, swim bladders evolved from lungs in some lineages. In nearly all ﬁshes, the skin is covered by ﬂattened, bony scales that differ in structure from the tooth-like scales of sharks. Glands in the skin secrete a slimy mucus over the skin, an adaptation that reduces drag during swimming. Like the ancient aquatic gnathostomes mentioned earlier, ﬁshes have a lateral line system, which is evident as a row of tiny pits in the skin on either side of the body. The details of ﬁsh reproduction vary extensively. Most species are oviparous, reproducing by external fertilization after the female sheds large numbers of small eggs. However, internal fertilization and birthing characterize other species. Swim bladder Dorsal fin Adipose fin (characteristic of trout) Brain Caudal fin Nostril Cut edge of operculum Anal fin Liver Gills Kidney Figure 34.16 Anatomy of a trout, a ray-ﬁnned ﬁsh. Lateral line Anus Heart Gonad Stomach Intestine Pelvic fin Urinary bladder CHAPTER 34 The Origin and Evolution of Vertebrates 707 Ray-Finned Fishes Nearly all the aquatic osteichthyans familiar to us are among the over 27,000 species of ray-ﬁnned ﬁshes (Actinopterygii) (Figure 34.17). Named for the bony rays that support their ﬁns, the ray-ﬁnned ﬁshes originated during the Silurian period (444–416 million years ago). The group has diversiﬁed greatly since that time, as suggested by modiﬁcations in body form and ﬁn structure that affect maneuvering, defense, and other functions (see Figure 34.17). Ray-ﬁnned ﬁshes serve as a major source of protein for humans, who have harvested them for thousands of years. However, industrial-scale ﬁshing operations appear to have driven some of the world’s biggest ﬁsheries to collapse. For example, after decades of abundant harvests, in the 1990s the catch of cod (Gadus morhua) in the northwest Atlantic plummeted to just 5% of its historic maximum, bringing codﬁshing there to a near halt. Despite ongoing restrictions on the ﬁshery, cod populations have yet to recover to sustainable levels. Ray-ﬁnned ﬁshes also face other pressures from humans, such as the diversion of rivers by dams. Changing water ﬂow patterns can hamper the ﬁshes’ ability to obtain food and interferes with migratory pathways and spawning grounds. Lobe-Fins Yellowfin tuna (Thunnus albacares) is a fast-swimming, schooling fish that is commercially important worldwide. Native to coral reefs of the Pacific Ocean, the brightly colored red lionfish (Pterois volitans) can inject venom through its spines, causing a severe and painful reaction in humans. Like the ray-ﬁnned ﬁshes, the other major lineage of osteichthyans, the lobe-ﬁns (Sarcopterygii), also originated during the Silurian period (Figure 34.18). The key derived character of lobe-ﬁns is the presence of rod-shaped bones surrounded by a thick layer of muscle in their pectoral and pelvic ﬁns. During the Devonian (416–359 million years ago), many lobe-ﬁns lived in brackish waters, such as in coastal wetlands. There they may have used their lobed ﬁns to swim and “walk” underwater across the substrate (as do some living lobe-ﬁns). Some Devonian lobe-ﬁns were gigantic predators. It is not uncommon to ﬁnd spike-shaped fossils of Devonian lobe-ﬁn teeth as big as your thumb. By the end of the Devonian period, lobe-ﬁn diversity was dwindling, and today only three lineages survive. One lineage, 5 cm Lower jaw The sea horse has a highly modified body form, as exemplified by Hippocampus ramulosus, shown above. Sea horses are unusual among animals in that the male carries the young during their embryonic development. The fine-spotted moray eel (Gymnothorax dovii) is a predator that ambushes prey from crevices in its coral reef habitat. Figure 34.17 Ray-ﬁnned ﬁshes (Actinopterygii). 708 UNIT FIVE The Evolutionary History of Biological Diversity Scaly covering Dorsal spine Figure 34.18 A reconstruction of an ancient lobe-ﬁn. Discovered in 2009, Guiyu oneiros is the earliest known lobe-ﬁn, dating to 420 million years ago. The fossil of this species was nearly complete, allowing for an accurate reconstruction. CONCEPT 34.5 Tetrapods are gnathostomes that have limbs Figure 34.19 A coelacanth (Latimeria). These lobe-ﬁns were found living off the coasts of southern Africa and Indonesia. One of the most signiﬁcant events in vertebrate history took place about 365 million years ago, when the ﬁns of some lobe-ﬁns evolved into the limbs and feet of tetrapods. Until then, all vertebrates had shared the same basic ﬁshlike anatomy. After tetrapods moved onto land, they took on many new forms, from leaping frogs to ﬂying eagles to bipedal humans. Derived Characters of Tetrapods the coelacanths (Actinistia), was thought to have become extinct 75 million years ago. However, in 1938, ﬁshermen caught a living coelacanth off the east coast of South Africa (Figure 34.19). Until the 1990s, all subsequent discoveries were near the Comoros Islands in the western Indian Ocean. Since 1999, coelacanths have also been found at various places along the eastern coast of Africa and in the eastern Indian Ocean, near Indonesia. The Indonesian population may represent a second species. The second lineage of living lobe-ﬁns, the lungﬁshes (Dipnoi), is represented today by six species in three genera, all of which are found in the Southern Hemisphere. Lungﬁshes arose in the ocean but today are found only in fresh water, generally in stagnant ponds and swamps. They surface to gulp air into lungs connected to their pharynx. Lungﬁshes also have gills, which are the main organs for gas exchange in Australian lungﬁshes. When ponds shrink during the dry season, some lungﬁshes can burrow into the mud and estivate (wait in a state of torpor; see Chapter 40). The third lineage of lobe-ﬁns that survives today is far more diverse than the coelacanths or the lungﬁshes. During the mid-Devonian, these organisms adapted to life on land and gave rise to vertebrates with limbs and feet, called tetrapods—a lineage that includes humans. The tetrapod clade is the topic of the next section. CONCEPT CHECK 34.4 1. What derived characters do sharks and tuna share? What are some characteristics that distinguish tuna from sharks? 2. Describe key adaptations of aquatic gnathostomes. 3. WHAT IF? Imagine that we could replay the history of life. Is it possible that a group of vertebrates that colonized land could have arisen from aquatic gnathostomes other than the lobe-ﬁns? Explain. For suggested answers, see Appendix A. The most signiﬁcant character of tetrapods gives the group its name, which means “four feet” in Greek. In place of pectoral and pelvic ﬁns, tetrapods have limbs with digits. Limbs support a tetrapod’s weight on land, while feet with digits efﬁciently transmit muscle-generated forces to the ground when it walks. Life on land brought numerous other changes to the tetrapod body plan. In tetrapods, the head is separated from the body by a neck that originally had one vertebra on which the skull could move up and down. Later, with the origin of a second vertebra in the neck, the head could also swing from side to side. The bones of the pelvic girdle, to which the hind legs are attached, are fused to the backbone, permitting forces generated by the hind legs against the ground to be transferred to the rest of the body. Except for some fully aquatic species (such as the axolotl discussed below), the adults of living tetrapods do not have gills; during embryonic development, the pharyngeal clefts instead give rise to parts of the ears, certain glands, and other structures. As you will see, some of these characters were dramatically altered or lost in various lineages of tetrapods. In birds, for example, the pectoral limbs became wings, and in whales, the entire body converged toward a ﬁshlike shape. The Origin of Tetrapods As you have read, the Devonian coastal wetlands were home to a wide range of lobe-ﬁns. Those that entered particularly shallow, oxygen-poor water could use their lungs to breathe air. Some species probably used their stout ﬁns to help them move across logs or the muddy bottom. Thus, the tetrapod body plan did not evolve “out of nowhere” but was simply a modiﬁcation of a preexisting body plan. The recent discovery of a fossil called Tiktaalik has provided new details on how this process occurred. Like a ﬁsh, this species had ﬁns, gills, and lungs, and its body was covered in scales. But unlike a ﬁsh, Tiktaalik had a full set of ribs CHAPTER 34 The Origin and Evolution of Vertebrates 709 Figure 34.20 ﬁsh and tetrapod characters. (Figure 34.21, on the facing page, includes an artist's conception of what Tiktaalik might have looked like.) I M PA C T Discovery of a “Fishapod”: Tiktaalik P aleontologists were on the hunt for fossils that could shed light on the evolutionary origin of tetrapods. Based on the ages of previously discovered fossils, researchers were looking for a dig site with rocks about 365–385 million years old. Ellesmere Island, in the Canadian Arctic, was one of the few such sites likely to contain fossils, because it was once a river. The search at this site was rewarded by the discovery of fossils of a 375-million-year-old lobe-ﬁn, named Tiktaalik. As shown in the chart and photographs below, Tiktaalik exhibits both Fish Characters Scales Fins Gills and lungs Tetrapod Characters Neck Ribs Fin skeleton Flat skull Eyes on top of skull WHY IT MATTERS As the most tetrapod-like ﬁsh known, Tiktaalik documents key steps in the vertebrate transition from water to land. Since Tiktaalik predates the oldest known tetrapod by 10 million years, its features suggest that key “tetrapod” traits, such as a wrist, ribs, and a neck, were in fact ancestral to the tetrapod lineage. The discovery also shows the predictive capacity of paleontology in identifying likely locations of fossils of interest. FURTHER READING E. B. Daeschler, N. H. Shubin, and F. A. Jenkins, A Devonian tetrapod-like ﬁsh and the evolution of the tetrapod body plan, Nature 440:757–763 (2006). MAKE CONNECTIONS Describe how Tiktaalik’s features illustrate Darwin’s concept of descent with modiﬁcation (see Concept 22.2, pp. 457–460). Shoulder bones Ribs Scales Neck Head Eyes on top of skull Humerus Ulna Flat skull “Wrist” Elbow Radius Fin that would have helped it breathe air and support its body (Figure 34.20). Also unlike a ﬁsh, Tiktaalik had a neck and shoulders, allowing it to move its head about. Finally, the bones of Tiktaalik’s front ﬁn have the same basic pattern found in all limbed animals: one bone (the humerus), followed by two bones (the radius and ulna), followed by a group of small bones that comprise the wrist. Although it is unlikely that Tiktaalik could walk on land, its front ﬁn skeleton suggests that it could prop itself up in water on its ﬁns. Tiktaalik and other extraordinary fossil discoveries have allowed paleontologists to reconstruct how ﬁns became progressively more limb-like over time, culminating in the appearance of the ﬁrst tetrapods 365 million years ago (Figure 34.21). Over the next 60 million years, a great diversity of tetrapods arose. Judging from the morphology and locations of their fossils, most of these early tetrapods probably 710 UNIT FIVE The Evolutionary History of Biological Diversity Fin skeleton remained tied to water, a characteristic they share with some members of a group of living tetrapods called amphibians. Amphibians The amphibians (class Amphibia) are represented today by about 6,150 species of salamanders (order Urodela, “tailed ones”), frogs (order Anura, “tail-less ones”), and caecilians (order Apoda, “legless ones”). About 550 species of urodeles are known. Some are entirely aquatic, but others live on land as adults or Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia Figure 34.21 Steps in the origin of limbs with digits. The white bars on the branches of this diagram place known fossils in time; arrowheads indicate lineages that extend to today. The drawings of extinct organisms are based on fossilized skeletons, but the colors are fanciful. Lungfishes Eusthenopteron WHAT IF? If the most recent common ancestor of Tulerpeton and living tetrapods originated 380 million years ago, what range of dates would include the origin of amphibians? Panderichthys Tiktaalik Acanthostega Tulerpeton Limbs with digits Amphibians Key to limb bones Ulna Radius Amniotes Humerus Silurian PALEOZOIC Carboniferous Devonian 415 400 385 370 355 340 325 Permian 310 295 280 265 0 Time (millions of years ago) throughout life. Most salamanders that live on land walk with a side-to-side bending of the body, a trait also found in early terrestrial tetrapods (Figure 34.22a). Paedomorphosis is common among aquatic salamanders; the axolotl, for instance, retains larval features even when it is sexually mature (see Figure 25.22). Anurans, numbering about 5,420 species, are more specialized than urodeles for moving on land (Figure 34.22b). Adult frogs use their powerful hind legs to hop along the terrain. Although often distinctive in appearance, the animals known as “toads” are simply frogs that have leathery skin or other adaptations for life on land. A frog nabs insects and other prey by ﬂicking out its long, sticky tongue, which is attached to the front of the mouth. Frogs display a great variety of adaptations that help them avoid being eaten by larger predators. Their skin glands secrete distasteful or even poisonous mucus. Many poisonous species have bright coloration, which predators apparently associate with danger (see Figure 54.5b). Other frogs have color patterns that camouﬂage them (see Figure 54.5a). (a) Order Urodela. Urodeles (salamanders) retain their tail as adults. Figure 34.22 Amphibians. (b) Order Anura. Anurans, such as this poison dart frog, lack a tail as adults. (c) Order Apoda. Apodans, or caecilians, are legless, mainly burrowing amphibians. CHAPTER 34 The Origin and Evolution of Vertebrates 711 Apodans, the caecilians (about 170 species), are legless and nearly blind, and superﬁcially they resemble earthworms (Figure 34.22c). Their absence of legs is a secondary adaptation, as they evolved from a legged ancestor. Caecilians inhabit tropical areas, where most species burrow in moist forest soil. A few South American species live in freshwater ponds and streams. Amphibian (derived from amphibious, meaning “both ways of life”) refers to the life stages of many frog species that live ﬁrst in water and then on land (Figure 34.23). The larval stage of a frog, called a tadpole, is usually an aquatic herbivore with gills, a lateral line system resembling that of aquatic vertebrates, and a long, ﬁnned tail. The tadpole initially lacks legs; it swims by undulating its tail. During the metamorphosis that leads to the “second life,” the tadpole develops legs, lungs, a pair of external eardrums, and a digestive system adapted to a carnivorous diet. At the same time, the gills disappear; the lateral line system also disappears in most species. The young frog crawls onto shore and becomes a terrestrial hunter. In spite of their name, however, many amphibians do not live a dual—aquatic and terrestrial—life. There are some strictly aquatic or strictly terrestrial frogs, salamanders, and caecilians. Moreover, salamander and caecilian larvae look much like the adults, and typically both the larvae and the adults are carnivorous. Most amphibians are found in damp habitats such as swamps and rain forests. Even those adapted to drier habitats spend much of their time in burrows or under moist leaves, where humidity is high. Amphibians generally rely heavily (a) The tadpole is an aquatic herbivore with a fishlike tail and internal gills. (b) During metamorphosis, the gills and tail are resorbed, and walking legs develop. The adult frog will live on land. (c) The adults return to water to mate. The male grasps the female, stimulating her to release eggs. The eggs are laid and fertilized in water. They have a jelly coat but lack a shell and would desiccate in air. Figure 34.23 The “dual life” of a frog (Rana temporaria). 712 UNIT FIVE The Evolutionary History of Biological Diversity on their moist skin for gas exchange with the environment. Some terrestrial species lack lungs and breathe exclusively through their skin and oral cavity. Fertilization is external in most amphibians; the male grasps the female and spills his sperm over the eggs as the female sheds them (see Figure 34.23c). Amphibians typically lay their eggs in water or in moist environments on land; the eggs lack a shell and dehydrate quickly in dry air. Some amphibian species lay vast numbers of eggs in temporary pools, and egg mortality is high. In contrast, other species lay relatively few eggs and display various types of parental care. Depending on the species, either males or females may house eggs on their back (Figure 34.24), in their mouth, or even in their stomach. Certain tropical tree frogs stir their egg masses into moist, foamy nests that resist drying. There are also some ovoviviparous and viviparous species that retain the eggs in the female reproductive tract, where embryos can develop without drying out. Many amphibians exhibit complex and diverse social behaviors, especially during their breeding seasons. Frogs are usually quiet, but the males of many species vocalize to defend their breeding territory or to attract females. In some species, migrations to speciﬁc breeding sites may involve vocal communication, celestial navigation, or chemical signaling. Over the past 30 years, zoologists have documented a rapid and alarming decline in amphibian populations in locations throughout the world. There appear to be several causes, including the spread of a disease-causing chytrid fungus (see Figure 31.26), habitat loss, climate change, and pollution. These and other factors have not only reduced populations, but led to extinctions. A recent study indicates that at least 9 amphibian species have become extinct since 1980; more than 100 other species have not been seen since that time and are considered possibly extinct. Figure 34.24 A mobile nursery. A female pygmy marsupial frog, Flectonotus pygmaeus, incubates her eggs in a pouch of skin on her back, helping to protect the eggs from predators. When the eggs hatch, the female deposits the tadpoles in water where they begin life on their own. CONCEPT CHECK 34.5 CONCEPT 1. Describe the origin of tetrapods and identify some of their key derived traits. 2. Some amphibians never leave the water, whereas others can survive in relatively dry terrestrial environments. Contrast the adaptations that facilitate these two lifestyles. 3. WHAT IF? Scientists think that amphibian populations may provide an early warning system of environmental problems. What features of amphibians might make them particularly sensitive to environmental problems? For suggested answers, see Appendix A. 34.6 Amniotes are tetrapods that have a terrestrially adapted egg The amniotes are a group of tetrapods whose extant members are the reptiles (including birds) and mammals (Figure 34.25). During their evolution, amniotes acquired a number of new adaptations to life on land. Derived Characters of Amniotes Amniotes are named for the major derived character of the clade, the amniotic egg, which contains four specialized membranes: the amnion, the chorion, the yolk sac, and the Parareptiles Turtles Crocodilians Archosaurs Reptiles Pterosaurs Saurischians Diapsids Dinosaurs Ornithischian dinosaurs Saurischian dinosaurs other than birds Birds ANCESTRAL AMNIOTE Plesiosaurs Ichthyosaurs Lepidosaurs Tuataras Squamates Synapsids Figure 34.25 A phylogeny of amniotes. Extant groups are named at the tips of the branches in boldface type. The dotted line of the turtle branch indicates the uncertain relationship of turtles to other reptiles. Turtles may be a sister Mammals group to parareptiles (as indicated by some morphological data), or they may be diapsids more closely related to lepidosaurs (as indicated by other morphological analyses) or to archosaurs (as indicated by many molecular studies). CHAPTER 34 Based on this phylogeny, DNA sequences in birds are likely most similar to DNA sequences in which other extant group of amniotes? Explain. ? The Origin and Evolution of Vertebrates 713 Figure 34.26 The amniotic egg. The embryos of reptiles and mammals form four extraembryonic membranes: the amnion, chorion, yolk sac, and allantois. This diagram shows these membranes in the shelled egg of a reptile. Extraembryonic membranes Allantois. The allantois is a disposal sac for certain metabolic wastes produced by the embryo. The membrane of the allantois also functions with the chorion as a respiratory organ. Chorion. The chorion and the membrane of the allantois exchange gases between the embryo and the air. Oxygen and carbon dioxide diffuse freely across the shell. Amnion. The amnion protects the embryo in a fluid-filled cavity that cushions against mechanical shock. Yolk sac. The yolk sac contains the yolk, a stockpile of nutrients. Blood vessels in the yolk sac membrane transport nutrients from the yolk into the embryo. Other nutrients are stored in the albumen (”egg white”). Embryo Amniotic cavity with amniotic fluid Yolk (nutrients) Shell allantois (Figure 34.26). Called extraembryonic membranes because they are not part of the body of the embryo itself, these membranes develop from tissue layers that grow out from the embryo. The amniotic egg is named for the amnion, which encloses a compartment of ﬂuid that bathes the embryo and acts as a hydraulic shock absorber. The other membranes in the egg function in gas exchange, the transfer of stored nutrients to the embryo, and waste storage. The amniotic egg was a key evolutionary innovation for terrestrial life: It allowed the embryo to develop on land in its own private “pond,” hence reducing the dependence of tetrapods on an aqueous environment for reproduction. In contrast to the shell-less eggs of amphibians, the amniotic eggs of most reptiles and some mammals have a shell. The shells of bird eggs are calcareous (made of calcium carbonate) and inﬂexible, while the eggshells of many other reptiles are leathery and ﬂexible. Either kind of shell signiﬁcantly slows dehydration of the egg in air, an adaptation that helped amniotes to occupy a wider range of terrestrial habitats than amphibians, their closest living relatives. (Seeds played a similar role in the evolution of land plants, as we discussed in Chapter 30.) Most mammals have dispensed with the eggshell over the course of their evolution, and the embryo avoids desiccation by developing within the amnion inside the mother’s body. Amniotes have acquired other key adaptations to life on land. For example, amniotes use their rib cage to ventilate their lungs. This method is more efﬁcient than throat-based ventilation, which amphibians use as a supplement to breathing through their skin. The increased efﬁciency of rib cage ventilation may 714 UNIT FIVE The Evolutionary History of Biological Diversity Albumen have allowed amniotes to abandon breathing through their skin and develop less permeable skin, thereby conserving water. Early Amniotes The most recent common ancestor of living amphibians and amniotes likely lived about 350 million years ago. No fossils of amniotic eggs have been found from that time, which is not surprising given how delicate they are. Thus, it is not yet possible to say when the amniotic egg evolved, although it must have existed in the last common ancestor of living amniotes, which all have amniotic eggs. Based on where their fossils have been found, the earliest amniotes lived in warm, moist environments, as did the ﬁrst tetrapods. Over time, however, early amniotes expanded into a wide range of new environments, including dry and highlatitude regions. The earliest amniotes were small and had sharp teeth, a sign that they were predators (Figure 34.27). Later groups also included herbivores, as evidenced by their grinding teeth and other features. Figure 34.27 Artist’s reconstruction of Hylonomus, an early amniote. About 25 cm long, this species lived 310 million years ago and probably ate insects and other small invertebrates. Reptiles The reptile clade includes tuataras, lizards, snakes, turtles, crocodilians, and birds, along with a number of extinct groups, such as plesiosaurs and ichthyosaurs (see Figure 34.25). Fossil evidence indicates that the earliest reptiles lived about 310 million years ago and resembled lizards. Reptiles have diverged greatly since that time, but as a group they share several derived characters that distinguish them from other tetrapods. For example, unlike amphibians, reptiles have scales that contain the protein keratin (as does a human nail). Scales help protect the animal’s skin from desiccation and abrasion. In addition, most reptiles lay their shelled eggs on land (Figure 34.28). Fertilization must occur internally, before the eggshell is secreted. Many species of snakes and lizards are viviparous; in such species, the extraembryonic membranes form a kind of placenta that enables the embryo to obtain nutrients from its mother. Reptiles such as lizards and snakes are sometimes described as “cold-blooded” because they do not use their metabolism extensively to control their body temperature. However, they do regulate their body temperature by using behavioral adaptations. For example, many lizards bask in the sun when the air is cool and seek shade when the air is too warm. A more accurate description of these reptiles is to say that they are ectothermic, which means that they absorb external heat as their main source of body heat. (This topic is discussed in more detail in Chapter 40.) By warming themselves directly with solar energy rather than through Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia Figure 34.28 Hatching reptiles. These bushmaster snakes (Lachesis muta) are breaking out of their parchment-like shells, a common type of shell among living reptiles other than birds. the metabolic breakdown of food, an ectothermic reptile can survive on less than 10% of the food energy required by a mammal of the same size. But the reptile clade is not entirely ectothermic; birds are endothermic, capable of maintaining body temperature through metabolic activity. The Origin and Evolutionary Radiation of Reptiles The oldest reptilian fossils, found in rocks from Nova Scotia, date from the late Carboniferous period. As reptiles diverged from their lizard-like ancestors, one of the ﬁrst major groups to emerge were the parareptiles, which were mostly large, stocky, quadrupedal herbivores. Some parareptiles had plates on their skin that may have provided them with defense against predators. Parareptiles died out by about 200 million years ago, at the end of the Triassic period. As parareptiles were dwindling, another ancient clade of reptiles, the diapsids, was diversifying. One of the most obvious derived characters of diapsids is a pair of holes on each side of the skull, behind the eye socket; muscles pass through these holes and attach to the jaw, controlling jaw movement. The diapsids are composed of two main lineages. One lineage gave rise to the lepidosaurs, which include tuataras, lizards, and snakes. This lineage also produced a number of marine reptiles, including the giant mososaurs. Some of these marine species rivaled today’s whales in length; all of them are extinct. (We’ll say more about living lepidosaurs shortly.) The other diapsid lineage, the archosaurs, produced the crocodilians (which we’ll discuss later), pterosaurs, and dinosaurs. Pterosaurs, which originated in the late Triassic, were the ﬁrst tetrapods to exhibit ﬂapping ﬂight. The pterosaur wing was completely different from the wings of birds and bats. It consisted of a collagen-strengthened membrane that stretched between the trunk or hind leg and a very long digit on the foreleg. Well-preserved fossils show evidence of muscles, blood vessels, and nerves in the wing membranes, suggesting that pterosaurs could dynamically adjust their membranes to assist their ﬂight. The smallest pterosaurs were no bigger than a sparrow, and the largest had a wingspan of nearly 11 m. They appear to have converged on many of the ecological roles later played by birds; some were insect-eaters, others grabbed ﬁsh out of the ocean, and still others ﬁltered small animals through thousands of ﬁne needlelike teeth. But by the end of the Cretaceous period 65 million years ago, pterosaurs had become extinct. On land, the dinosaurs diversiﬁed into a vast range of shapes and sizes, from bipeds the size of a pigeon to 45-m-long quadrupeds with necks long enough to let them browse the tops of trees. One lineage of dinosaurs, the ornithischians, were herbivores; they included many species with elaborate defenses against predators, such as tail clubs and horned crests. The other main lineage of dinosaurs, the saurischians, included the CHAPTER 34 The Origin and Evolution of Vertebrates 715 long-necked giants and a group called the theropods, which were bipedal carnivores. Theropods included the famous Tyrannosaurus rex as well as the ancestors of birds. There is continuing debate about the metabolism of dinosaurs. Some researchers have pointed out that the Mesozoic climate over much of the dinosaurs’ range was relatively warm and unvarying, and they have suggested that the low Figure 34.29 Extant reptiles (other than birds). (a) Tuatara (Sphenodon punctatus) (b) Australian thorny devil lizard (Moloch horridus) surface-to-volume ratios of large dinosaurs combined with behavioral adaptations such as basking may have been sufﬁcient for an ectotherm to maintain a suitable body temperature. However, some anatomical evidence supports the hypothesis that at least some dinosaurs were endotherms. Furthermore, paleontologists have found fossils of dinosaurs in both Antarctica and the Arctic; although the climate in these areas was milder when dinosaurs existed than it is today, it was cool enough that small dinosaurs may have had difﬁculty maintaining a high body temperature through ectothermy. The dinosaur that gave rise to birds was certainly endothermic, as are all birds. Traditionally, dinosaurs were considered slow, sluggish creatures. Since the early 1970s, however, fossil discoveries and research have led to the conclusion that many dinosaurs were agile and fast moving. Dinosaurs had a limb structure that enabled them to walk and run more efﬁciently than could earlier tetrapods, which had a sprawling gait. Fossilized footprints and other evidence suggest that some species were social—they lived and traveled in groups, much as many mammals do today. Paleontologists have also discovered evidence that some dinosaurs built nests and brooded their eggs, as birds do today (see Figure 26.17). All dinosaurs except birds became extinct by the end of the Cretaceous period. Their extinction may have been caused at least in part by the asteroid or comet impact you read about in Chapter 25. Some analyses of the fossil record are consistent with this idea in that they show a sudden decline in dinosaur diversity at the end of the Cretaceous. However, other analyses indicate that the number of dinosaur species had begun to decline several million years before the Cretaceous ended. Further fossil discoveries and new analyses will be needed to resolve this debate. Lepidosaurs (c) Wagler’s pit viper (Tropidolaemus wagleri) (d) Eastern box turtle (Terrapene carolina carolina) (e) American alligator (Alligator mississippiensis) 716 UNIT FIVE The Evolutionary History of Biological Diversity One surviving lineage of lepidosaurs is represented by two species of lizard-like reptiles called tuataras (Figure 34.29a). Fossil evidence indicates that tuatara ancestors lived at least 220 million years ago. These organisms thrived on many continents well into the Cretaceous period, reaching up to a meter in length. Today, however, tuataras are found only on 30 islands off the coast of New Zealand. When humans arrived in New Zealand 750 years ago, the rats that accompanied them devoured tuatara eggs, eventually eliminating the reptiles on the main islands. The tuataras that remain on the outlying islands are about 50 cm long and feed on insects, small lizards, and bird eggs and chicks. They can live to be over 100 years old. Their future survival depends on whether their remaining habitats are kept rat-free. The other major living lineage of lepidosaurs consists of the lizards and snakes, or squamates, which number about 7,900 species. Lizards are the most numerous and diverse reptiles (apart from birds) alive today (Figure 34.29b). Many lizards are small; the Jaragua lizard, discovered in the Dominican Republic in 2001, is only 16 mm long—small enough to ﬁt comfortably on a dime. In contrast, the Komodo dragon of Indonesia is a lizard that can reach a length of 3 m. It hunts deer and other large prey, delivering venom with its bite. Snakes are legless lepidosaurs (Figure 34.29c). As described in Chapter 26, snakes descended from lizards with legs. Today, some species of snakes retain vestigial pelvic and limb bones, providing evidence of their ancestry. Despite their lack of legs, snakes are quite proﬁcient at moving on land, most often by producing waves of lateral bending that pass from head to tail. Force exerted by the bends against solid objects pushes the snake forward. Snakes can also move by gripping the ground with their belly scales at several points along the body while the scales at intervening points are lifted slightly off the ground and pulled forward. Snakes are carnivorous, and a number of adaptations aid them in hunting and eating prey. They have acute chemical sensors, and though they lack eardrums, they are sensitive to ground vibrations, which helps them detect the movements of prey. Heat-detecting organs between the eyes and nostrils of pit vipers, including rattlesnakes, are sensitive to minute temperature changes, enabling these night hunters to locate warm animals. Venomous snakes inject their toxin through a pair of sharp teeth that may be hollow or grooved. The ﬂicking tongue is not venomous but helps fan odors toward olfactory (smell) organs on the roof of the mouth. Loosely articulated jawbones and elastic skin enable most snakes to swallow prey larger than the diameter of the snake’s head (see Figure 23.14). Turtles Turtles are one of the most distinctive group of reptiles alive today. All turtles have a boxlike shell made of upper and lower shields that are fused to the vertebrae, clavicles (collarbones), and ribs (Figure 34.29d). Most of the 307 known species of turtles have a hard shell, providing excellent defense against predators. A 2008 study reported the discovery of the oldest known fossil of the turtle lineage, dating to 220 million years ago. This fossil has a complete lower shell but an incomplete upper shell, suggesting that turtles may have acquired full shells in stages. The marine sediments in which this fossil was found also suggest that turtles may have originated in shallow coastal waters. However, as other scientists have argued, it is also possible that turtles originated on land and that the incomplete upper shell of this fossil may have been a specialized adaptation for an aquatic lifestyle. Scientists continue to hunt for fossils that could shed light on the origin of the turtle shell. The earliest turtles could not retract their head into their shell, but mechanisms for doing so evolved independently in two separate branches of turtles. The side-necked turtles fold their neck horizontally, while the vertical-necked turtles fold their neck vertically. Some turtles have adapted to deserts, and others live almost entirely in ponds and rivers. Still others have returned to the sea. Sea turtles have a reduced shell and enlarged forelimbs that function as ﬂippers. They include the largest living turtles, the deep-diving leatherbacks, which can exceed a mass of 1,500 kg and feed on jellies. Leatherbacks and other sea turtles are endangered by being caught in ﬁshing nets, as well as by development of the beaches where the turtles lay their eggs. Alligators and Crocodiles Alligators and crocodiles (collectively called crocodilians) belong to a lineage that reaches back to the late Triassic (Figure 34.29e). The earliest members of this lineage were small terrestrial quadrupeds with long, slender legs. Later species became larger and adapted to aquatic habitats, breathing air through their upturned nostrils. Some Mesozoic crocodilians grew as long as 12 m and may have attacked dinosaurs and other prey at the water’s edge. The 23 known species of living crocodilians are conﬁned to warm regions of the globe. Alligators in the southeastern United States have made a comeback after spending years on the endangered species list. Birds There are about 10,000 species of birds in the world. Like crocodilians, birds are archosaurs, but almost every feature of their anatomy has been modiﬁed in their adaptation to ﬂight. Derived Characters of Birds Many of the characters of birds are adaptations that facilitate ﬂight, including weight-saving modiﬁcations that make ﬂying more efﬁcient. For example, birds lack a urinary bladder, and the females of most species have only one ovary. The gonads of both females and males are usually small, except during the breeding season, when they increase in size. Living birds are also toothless, an adaptation that trims the weight of the head. CHAPTER 34 The Origin and Evolution of Vertebrates 717 Finger 1 (b) Bone structure Palm (a) Wing Finger 2 Finger 3 Forearm Wrist Shaft Vane Shaft Barb Barbule Hook (c) Feather structure A bird’s most obvious adaptations for ﬂight are its wings and feathers (Figure 34.30). Feathers are made of the protein β-keratin, which is also found in the scales of other reptiles. The shape and arrangement of the feathers form the wings into airfoils, and they illustrate some of the same principles of aerodynamics as the wings of an airplane. Power for ﬂapping the wings comes from contractions of large pectoral (breast) muscles anchored to a keel on the sternum (breastbone). Some birds, such as eagles and hawks, have wings adapted for soaring on air currents and ﬂap their wings only occasionally; other birds, including hummingbirds, must ﬂap continuously to stay aloft (see Figure 34.34). Among the fastest birds are the appropriately named swifts, which can ﬂy up to 170 km/hr. Flight provides numerous beneﬁts. It enhances hunting and scavenging; many birds consume ﬂying insects, an abundant, highly nutritious food resource. Flight also provides ready escape from earthbound predators and enables some birds to migrate great distances to exploit different food resources and seasonal breeding areas. Flying requires a great expenditure of energy from an active metabolism. Birds are endothermic; they use their own metabolic heat to maintain a high, constant body temperature. Feathers and in some species a layer of fat provide insulation that enables birds to retain body heat. The lungs have 718 UNIT FIVE The Evolutionary History of Biological Diversity Figure 34.30 Form ﬁts function: the avian wing and feather. (a) A wing is a remodeled version of the tetrapod forelimb. (b) The bones of many birds have a honeycombed internal structure and are ﬁlled with air. (c) A feather consists of a central air-ﬁlled shaft, from which radiate the vanes. The vanes are made up of barbs, which bear small branches called barbules. Birds have contour feathers and downy feathers. Contour feathers are stiff and contribute to the aerodynamic shapes of the wings and body. Their barbules have hooks that cling to barbules on neighboring barbs. When a bird preens, it runs the length of each contour feather through its bill, engaging the hooks and uniting the barbs into a precise shape. Downy feathers lack hooks, and the free-form arrangement of their barbs produces a ﬂufﬁness that provides insulation by trapping air. tiny tubes leading to and from elastic air sacs that improve airﬂow and oxygen uptake. This efﬁcient respiratory system and a circulatory system with a four-chambered heart keep tissues well supplied with oxygen and nutrients, supporting a high rate of metabolism. Flight also requires both acute vision and ﬁne muscle control. Birds have color vision and excellent eyesight. The visual and motor areas of the brain are well developed, and the brain is proportionately larger than those of amphibians and nonbird reptiles. Birds generally display very complex behaviors, particularly during breeding season, when they engage in elaborate courtship rituals. Because eggs have shells by the time they are laid, fertilization must be internal. Copulation usually involves contact between the mates’ vents, the openings to their cloacas. After eggs are laid, the avian embryo must be kept warm through brooding by the mother, the father, or both, depending on the species. The Origin of Birds Cladistic analyses of birds and reptilian fossils indicate that birds belong to the group of bipedal saurischian dinosaurs called theropods. Since the late 1990s, Chinese paleontologists have unearthed a spectacular trove of feathered theropod fossils that are shedding light on the origin of birds. Several species of dinosaurs closely related to birds had feathers with vanes, and a wider range of species had ﬁlamentous feathers. Such ﬁndings imply that feathers evolved long before powered ﬂight. Among the possible functions of these early feathers were insulation, camouﬂage, and courtship display. How did ﬂight evolve in the theropods? In one scenario, feathers may have enabled small, running dinosaurs chasing prey or escaping predators to gain extra lift as they jumped into the air. Or small dinosaurs could have gained traction as they ran up hills by ﬂapping their feathered forelimbs—a behavior seen in some birds today. In a third scenario, some dinosaurs could have climbed trees and glided, aided by feathers. Whether birds took to the air from the ground up or the trees down, an essential question being studied by scientists ranging from paleontologists to engineers is how their efﬁcient ﬂight stroke evolved. By 150 million years ago, feathered theropods had evolved into birds. Archaeopteryx, which was discovered in a German limestone quarry in 1861, remains the earliest known bird (Figure 34.31). It had feathered wings but retained ancestral characters such as teeth, clawed digits in its wings, and a long tail. Archaeopteryx ﬂew well at high speeds, but unlike a present-day bird, it could not take off from a standing position. Fossils of later birds from the Cretaceous show a gradual loss of certain ancestral dinosaur features, such as teeth and clawed forelimbs, as well as the acquisition of innovations found in extant birds, including a short tail covered by a fan of feathers. Toothed beak Airfoil wing with contour feathers Wing claw Figure 34.32 An emu (Dromaius novaehollandiae), a ﬂightless bird native to Australia. Living Birds Clear evidence of Neornithes, the clade that includes the 28 orders of living birds, can be found before the Cretaceous-Paleogene boundary 65.5 million years ago. Several groups of living and extinct birds include one or more ﬂightless species. The ratites (order Struthioniformes), which consist of the ostrich, rhea, kiwi, cassowary, and emu, are all ﬂightless (Figure 34.32). In ratites, the sternal keel is absent, and the pectoral muscles are small relative to those of birds that can ﬂy. Penguins make up the ﬂightless order Sphenisciformes, but, like ﬂying birds, they have powerful pectoral muscles. They use these muscles to “ﬂy” in the water: As they swim, they ﬂap their ﬂipper-like wings in a manner that resembles the ﬂight stroke of a more typical bird (Figure 34.33). Certain species of rails, ducks, and pigeons are also ﬂightless. Although the demands of ﬂight have rendered the general body forms of many ﬂying birds similar to one another, experienced bird-watchers can distinguish species by their proﬁle, colors, ﬂying style, behavior, and beak shape. The skeleton of a hummingbird wing is unique, making them the only birds Long tail with many vertebrae Figure 34.31 Artist’s reconstruction of Archaeopteryx, the earliest known bird. Fossil evidence indicates that Archaeopteryx was capable of powered ﬂight but retained many characters of nonbird dinosaurs. Figure 34.33 A king penguin (Aptenodytes patagonicus) “ﬂying” underwater. With their streamlined shape and powerful pectoral muscles, penguins are fast and agile swimmers. CHAPTER 34 The Origin and Evolution of Vertebrates 719 Figure 34.34 Hummingbird feeding while hovering. A hummingbird can rotate its wings in all directions, enabling it to hover and ﬂy backwards. CONCEPT CHECK 34.6 1. Describe three key amniote adaptations for life on land. 2. Are snakes tetrapods? Explain. 3. Identify four avian adaptations for ﬂight. 4. WHAT IF? Suppose turtles are more closely related to lepidosaurs than to other reptiles. Redraw Figure 34.25 to show this relationship, and mark the node that represents the most recent common ancestor shared by all living reptiles. Deﬁning the reptile clade as consisting of all descendants of that ancestor, list the reptiles. For suggested answers, see Appendix A. that can hover and ﬂy backwards (Figure 34.34). Adult birds lack teeth, but during the course of avian evolution their beaks have taken on a variety of shapes suited to different diets. Some birds, such as parrots, have crushing beaks with which they can crack open hard nuts and seeds. Other birds, such as ﬂamingoes, are ﬁlter feeders. Their beaks have remarkable ‘strainers’ that enable them to capture food particles from the water (Figure 34.35). Foot structure, too, shows considerable variation. Various birds use their feet for perching on branches (Figure 34.36), grasping food, defense, swimming or walking, and even courtship (see Figure 24.3e). CONCEPT 34.7 Mammals are amniotes that have hair and produce milk Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Amphibia Reptilia Mammalia The reptiles we have been discussing represent one of the two living lineages of amniotes. The other amniote lineage is our own, the mammals (class Mammalia). Today, there are more than 5,300 known species of mammals on Earth. Derived Characters of Mammals Figure 34.35 Specialized beaks. This greater ﬂamingo (Phoenicopterus ruber) dips its beak into the water and strains out the food. Figure 34.36 Feet adapted to perching. This great tit (Parus major) is a member of the Passeriformes, the perching birds. The toes of these birds can lock around a branch or wire, enabling the bird to rest for long periods. 720 UNIT FIVE The Evolutionary History of Biological Diversity The distinctive character from which mammals derive their name is their mammary glands, which produce milk for offspring. All mammalian mothers nourish their young with milk, a balanced diet rich in fats, sugars, proteins, minerals, and vitamins. Hair, another mammalian characteristic, and a fat layer under the skin help the body retain heat. Like birds, mammals are endothermic, and most have a high metabolic rate. Efﬁcient respiratory and circulatory systems (including a four-chambered heart) support a mammal’s metabolism. A sheet of muscle called the diaphragm helps ventilate the lungs. Like birds, mammals generally have a larger brain than other vertebrates of equivalent size, and many species are capable learners. And as in birds, the relatively long duration of parental care extends the time for offspring to learn important survival skills by observing their parents. Differentiated teeth are another important mammalian trait. Whereas the teeth of reptiles are generally uniform in size and shape, the jaws of mammals bear a variety of teeth with sizes and shapes adapted for chewing many kinds of foods. Humans, like most mammals, have teeth modiﬁed for shearing (incisors and canine teeth) and for crushing and grinding (premolars and molars; see Figure 41.16). from other amniotes. They were small and probably hairy, and they likely fed on insects at night. Their bones show that they grew faster than other synapsids, suggesting that they probably had a relatively high metabolic rate; however, they still laid eggs. During the Jurassic (200–145 million years ago), the ﬁrst true mammals arose and diversiﬁed into many short-lived lineages. A diverse set of mammal species coexisted with dinosaurs in Jurassic and Cretaceous periods, but these species were not abundant or dominant members of their community, and most measured less than 1 m. One possible explanation for their small size is that dinosaurs already occupied ecological niches of large-bodied animals. By the early Cretaceous, the three major lineages of mammals had emerged: those leading to monotremes (egg-laying mammals), marsupials (mammals with a pouch), and eutherians (placental mammals). After the extinction of large dinosaurs, pterosaurs, and marine reptiles during the late Cretaceous period, mammals underwent an adaptive radiation, giving rise to large predators and herbivores as well as ﬂying and aquatic species. Early Evolution of Mammals Mammals belong to a group of amniotes known as synapsids. Early nonmammalian synapsids lacked hair, had a sprawling gait, and laid eggs. A distinctive characteristic of synapsids is the single temporal fenestra, a hole behind the eye socket on each side of the skull. Humans retain this feature; your jaw muscles pass through the temporal fenestra and anchor on your temple. Fossil evidence shows that the jaw was remodeled as mammalian features arose gradually in successive lineages of earlier synapsids (see Figure 25.6); in all, these changes took more than 100 million years. In addition, two of the bones that formerly made up the jaw joint were incorporated into the mammalian middle ear (Figure 34.37). This evolutionary change is reﬂected in changes that occur during development. For example, as a mammalian embryo grows, the posterior region of its jaw— which in a reptile forms the articular bone—can be observed to detach from the jaw and migrate to the ear, where it forms the malleus. Synapsids evolved into large herbivores and carnivores during the Permian period, and for a time they were the dominant tetrapods. However, the Permian-Triassic extinctions took a heavy toll on them, and their diversity fell during the Triassic (251–200 million years ago). Increasingly mammal-like synapsids emerged by the end of the Triassic. While not true mammals, these synapsids had acquired a number of the derived characters that distinguish mammals Biarmosuchus, a synapsid Monotremes Monotremes are found only in Australia and New Guinea and are represented by one species of platypus and four species of echidnas (spiny anteaters). Monotremes lay eggs, a character that is ancestral for amniotes and retained in most Figure 34.37 The evolution of the mammalian ear bones. Biarmosuchus was a synapsid, a lineage that eventually gave rise to the mammals. Bones that transmit sound in the ear of mammals arose from the modiﬁcation of bones in the jaw of nonmammalian synapsids. Key Articular Temporal fenestra Quadrate Dentary Jaw joint MAKE CONNECTIONS Review the deﬁnition of exaptation in Concept 25.6 (p. 530). Summarize the process by which exaptation occurs and explain how the incorporation of the articular and quadrate bones into the mammalian inner ear is an example. Squamosal (a) In Biarmosuchus, the articular and quadrate bones formed the jaw joint. Middle ear Eardrum Stapes Eardrum Inner ear Middle ear Inner ear Stapes Sound Sound Incus (quadrate) Malleus (articular) Present-day reptile Present-day mammal (b) During the evolutionary remodeling of the mammalian skull, a new jaw joint formed between the dentary and squamosal bones (see Figure 25.6). No longer used in the jaw, the quadrate and articular bones became incorporated into the middle ear as two of the three bones that transmit sound from the eardrum to the inner ear. CHAPTER 34 The Origin and Evolution of Vertebrates 721 Figure 34.38 Short-beaked echidna (Tachyglossus aculeatus), an Australian monotreme. Monotremes have hair and produce milk, but they lack nipples. Monotremes are the only mammals that lay eggs (inset). (a) A young brushtail possum. The offspring of marsupials are born very early in their development. They finish their growth while nursing from a nipple (in their mother’s pouch in most species). reptiles (Figure 34.38). Like all mammals, monotremes have hair and produce milk, but they lack nipples. Milk is secreted by glands on the belly of the mother. After hatching, the baby sucks the milk from the mother’s fur. Marsupials Opossums, kangaroos, and koalas are examples of marsupials. Both marsupials and eutherians share derived characters not found among monotremes. They have higher metabolic rates and nipples that provide milk, and they give birth to live young. The embryo develops inside the uterus of the female’s reproductive tract. The lining of the uterus and the extraembryonic membranes that arise from the embryo form a placenta, a structure in which nutrients diffuse into the embryo from the mother’s blood. A marsupial is born very early in its development and completes its embryonic development while nursing. In most species, the nursing young are held within a maternal pouch called a marsupium (Figure 34.39a). A red kangaroo, for instance, is about the size of a honeybee at its birth, just 33 days after fertilization. Its back legs are merely buds, but its front legs are strong enough for it to crawl from the exit of its mother’s reproductive tract to a pouch that opens to the front of her body, a journey that lasts a few minutes. In other species, the marsupium opens to the rear of the mother’s body; in bandicoots, this protects the young as their mother burrows in the dirt (Figure 34.39b). Marsupials existed worldwide during the Mesozoic era, but today they are found only in the Australian region and in North and South America. The biogeography of marsupials is an example of the interplay between biological and geologic evolution (see Concept 25.4). After the breakup of the supercontinent Pangaea, South America and Australia became island 722 UNIT FIVE The Evolutionary History of Biological Diversity (b) Long-nosed bandicoot. Most bandicoots are diggers and burrowers that eat mainly insects but also some small vertebrates and plant material. Their rear-opening pouch helps protect the young from dirt as the mother digs. Other marsupials, such as kangaroos, have a pouch that opens to the front. Figure 34.39 Australian marsupials. continents, and their marsupials diversiﬁed in isolation from the eutherians that began an adaptive radiation on the northern continents. Australia has not been in contact with another continent since early in the Cenozoic era, about 65 million years ago. In Australia, convergent evolution has resulted in a diversity of marsupials that resemble eutherians in similar ecological roles in other parts of the world (Figure 34.40). In contrast, although South America had a diverse marsupial fauna throughout the Paleogene, it has experienced several migrations of eutherians. One of the most important migrations occurred about 3 million years ago, when North and South America joined at the Panamanian isthmus and extensive twoway trafﬁc of animals took place over the land bridge. Today, only three families of marsupials live outside the Australian region, and the only marsupials found in the wild in North America are a few species of opossum. Marsupial mammals Plantigale Eutherians (Placental Mammals) Eutherian mammals Deer mouse Marsupial mole Sugar glider Mole Flying squirrel Eutherians are commonly called placental mammals because their placentas are more complex than those of marsupials. Eutherians have a longer pregnancy than marsupials. Young eutherians complete their embryonic development within the uterus, joined to their mother by the placenta. The eutherian placenta provides an intimate and long-lasting association between the mother and her developing young. The major groups of living eutherians are thought to have diverged from one another in a burst of evolutionary change. The timing of this burst is uncertain: It is dated to 100 million years ago by molecular data and 60 million years ago by morphological data. Figure 34.41, on the next two pages, explores the major eutherian orders and their possible phylogenetic relationships with each other as well as with the monotremes and marsupials. Primates The mammalian order Primates includes the lemurs, tarsiers, monkeys, and apes. Humans are members of the ape group. Wombat Woodchuck Tasmanian devil Kangaroo Wolverine Patagonian cavy Figure 34.40 Convergent evolution of marsupials and eutherians (placental mammals). (Drawings are not to scale.) Derived Characters of Primates Most primates have hands and feet adapted for grasping, and their digits have ﬂat nails instead of the narrow claws of other mammals. There are other characteristic features of the hands and f

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