Chapter 34 - Vertebrates

Chapter 34 Vertebrates
Lecture Outline

Overview: Half a Billion Years of Backbones

• Vertebrates are named for vertebrae, the series of bones that make up the vertebral column or backbone.
• There are about 52,000 species of vertebrates, far fewer than the 1 million insect species on Earth.
  • Plant-eating dinosaurs, at 40,000 kg, were the heaviest animals to walk on land.
  • The biggest animal that ever existed is the blue whale, at 100,000 kg.
  • Humans and our closest relatives are vertebrates.
• This group includes other mammals, birds, lizards, snakes, turtles, amphibians, and the various classes of fishes.

Concept 34.1 Chordates have a notochord and a dorsal, hollow nerve cord

• The vertebrates belong to one of the two major phyla in the Deuterostomia, the chordates.
  • Chordates are bilaterian animals, belonging to the Deuterostomia.
• The phylum Chordata includes three subphyla, the vertebrates and two phyla of invertebrates—the urochordates and the cephalochordates.

  Four derived characters define the phylum Chordata.

• Although chordates vary widely in appearance, all share the presence of four anatomical structures at some point in their lifetime.
• These chordate characteristics are a notochord; a dorsal, hollow nerve cord; pharyngeal slits; and a muscular, post-anal tail.
  1. The notochord, present in all chordate embryos, 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.
     • It provides skeletal support throughout most of the length of the animal.
     • While the notochord persists in the adult stage of some invertebrate chordates and primitive vertebrates, it remains only as a remnant in vertebrates with a more complex, jointed skeleton.
     • For example, it is the gelatinous material of the disks between vertebrae in humans.
  2. The dorsal, hollow nerve cord of a chordate embryo develops from a plate of ectoderm that rolls into a tube dorsal to the notochord.
     • Other animal phyla have solid nerve cords, usually located ventrally.
     • The nerve cord of the chordate embryo develops into the central nervous system: the brain and spinal cord.
  3. The digestive tube of chordates extends from the mouth to the anus.
     • The region 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 pharyngeal gill slits that allow water that enters the mouth to exit without continuing through the entire digestive tract.
     • In many invertebrate chordates, the pharyngeal gill slits function as suspension-feeding devices.
     • The slits and the structures that support them have become modified for gas exchange (in aquatic vertebrates), jaw support, hearing, and other functions during vertebrate evolution.
  4. Most chordates have a muscular tail extending posterior to the anus.
     • In contrast, nonchordates have a digestive tract that extends nearly the whole length of the body.
     • The chordate tail contains skeletal elements and muscles.
     • It provides much of the propulsive force in many aquatic species.

  Invertebrate chordates provide clues to the origin of vertebrates.

• Members of the subphylum Urochordata, commonly called tunicates, belong to the deepest-branching lineage of chordates.
  • They most resemble chordates during their larval stage, which may be brief.
• The tunicate larva uses its tail muscles and notochord to swim through the water in search of a suitable substrate on which it can settle, guided by cues from light- and gravity-sensitive cells.
• Tunicates undergo a radical metamorphosis to form a sessile adult with few chordate characteristics.
  • Its tail and notochord are resorbed, its nervous system degenerates, and its organs rotate 90 degrees.
• Tunicates are suspension feeders.
  • Seawater passes inside the animal via an incurrent siphon, through the pharyngeal gill slits, and into a ciliated chamber, the atrium.
  • Food filtered from the water is trapped by a mucous net that is passed by cilia into the intestine.
  • Filtered water and feces exit through an anus that empties into an excurrent siphon.
• Lancelets (members of the subphylum Cephalochordata) are blade-like in shape.
  • The notochord; dorsal, hollow nerve cord; numerous gill slits; and post-anal tail all persist in the adult stage.
  • Lancelets are up to 5 cm long.
  • They live with their posterior end buried in the sand and the anterior end exposed for feeding.
• Adult lancelets retain key chordate characteristics.
• Lancelets are suspension feeders, feeding by trapping tiny particles on mucous nets secreted across the pharyngeal slits.
  • Ciliary pumping creates a flow of water with suspended food particles into the mouth and out the gill slits.
  • In lancelets, the pharynx and gill slits are feeding structures and play only a minor role in respiration, which primarily occurs across the external body surface.
• A lancelet frequently leaves its burrow to swim to a new location.
• Though feeble swimmers, their swimming mechanism resembles that of fishes through the coordinated contraction of serial muscle blocks.
  • Contraction of chevron-shaped muscles flexes the notochord and produces lateral undulations that thrust the body forward.
  • The muscle segments develop from blocks of mesoderm, called somites, arranged serially along each side of the notochord of the embryo.
• Tunicates and lancelets may provide clues about the evolutionary origin of the vertebrate body plan.
• Tunicates display a number of chordate characteristics only as larvae, while lancelets retain those characters as adults.
  • Thus, an adult lancelet looks more like a larval tunicate than like an adult tunicate.
• In the 1920s, biologist William Garstang suggested that tunicates represent an early stage in chordate evolution.
  • This stage may have occurred through paedogenesis, the precocious development of sexual maturity in a larva.
  • Garstang proposed that ancestral chordates became sexually mature while still in the larval stage.
• The paedogenetic hypothesis is deduced from comparing modern forms, but the weight of evidence is against it.
• The degenerate adult stage of tunicates appears to be a derived trait that evolved only after the tunicate lineage branched off from other chordates.
  • Even the tunicate larva appears to be highly derived.
  • Studies of Hox gene expression suggest that the tunicate larva does not develop the posterior part of its body axis.
    • Rather, the anterior region is elongated and contains a heart and digestive system.
• Research on lancelets has revealed important clues about the evolution of the chordate brain.
  • Rather than a full-fledged brain, lancelets have only a slightly swollen tip on the anterior end of the dorsal nerve cord.
  • The same genes that organize major regions of the forebrain, midbrain, and hindbrain of vertebrates express themselves in a corresponding pattern in this small cluster of cells in the lancelet’s nerve cord.
  • The vertebrate brain apparently is an elaboration of an ancestral structure similar to the lancelet’s simple nerve cord tip.

Concept 34.2 Craniates are chordates that have a head

• After the evolution of the basic chordate body plan, the next major transition was the appearance of a head.
• Chordates with a head are known as craniates.
• The origin of a head—with a brain at the anterior end of the dorsal nerve cord, eyes and other sensory organs, and a skull—opened up a new way of feeding for chordates: active predation.

  Living craniates have a set of derived characters.

• Living craniates share a set of derived characters that distinguishes them from other chordates.
• On the genetic level, they possess two clusters of Hox genes, while lancelets and chordates have only one.
  • Other important families of genes that produce signaling molecules and transcription factors are also duplicated in craniates.
  • This additional genetic complexity made a more complex morphology possible.
• In craniates, a group of embryonic cells called the neural crest forms near the dorsal margins of the closing neural tube.
  • Neural crest cells disperse through the body and contribute to the formation of various structures, such as teeth, some of the bones and cartilages of the skull, the dermis of the face, several types of neurons, and the sensory capsules of the eyes and other sense organs.
  • The vertebrate cranium and brain (the enlarged anterior end of the dorsal, hollow nerve cord) and the anterior sensory organs are evidence of a high degree of cephalization, the concentration of sensory and neural equipment in the head.
• In 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 the slits.
  • This pumping sucks in food and facilitates gas exchange.

  Cambrian fossils provide clues to craniate origins.

• Several recent fossil finds in China of early chordates have provided information about the origin of craniates.
  • They appear to be “missing links” that straddle the transition to craniates.
  • The most primitive of these fossils is a 3-cm-long animal called Haikouella.
    • This animal resembles a lancelet and was probably a suspension feeder.
    • Haikouella also had a small but well-formed brain, eyes, and muscular segments.
    • It also had hardened structures (“denticles”) in the pharynx that may have functioned somewhat like teeth.
    • However, Haikouella did not have a skull.
  • In other Cambrian rocks, paleontologists have found fossils of more advanced chordates, such as Haikouichthys.
    • Haikouichthys had a skull composed of cartilage and is the oldest known true craniate.
  • These fossils push craniate origins back to the Cambrian explosion.

  Class Myxini: Hagfishes are the least derived craniate lineage.

• Hagfishes have a skull of cartilage but 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.
  • They have toothlike formations made of keratin.
• All of the 30 or so species of hagfishes are marine scavengers, feeding on worms and sick or dead fish.
  • Rows of slime glands along a hagfish’s body produce small amounts of slime perhaps to repulse other scavengers or larger amounts to deter a potential predator.
• Vertebrate systematists do not consider hagfishes to be fish.
  • The taxonomic term fish refers only to a specific clade of vertebrates, the actinopterygians.

Concept 34.3 Vertebrates are craniates that have a backbone

• During the Cambrian period, a lineage of craniates evolved into vertebrates.
• With a more complex nervous system and a more elaborate skeleton, vertebrates became active predators.
• After vertebrates branched off from other craniates, they underwent another genetic duplication, this one involving a group of transcription factor genes called the Dlx family.
• This additional genetic complexity was associated with innovations in vertebrate nervous systems and skeletons, including a more extensive skull and a backbone composed of vertebrae.
• In the majority of vertebrates, the vertebrae enclose the spinal cord and have taken over the biomechanical roles of the notochord.
• Aquatic vertebrates also have a number of adaptations associated with faster swimming, including fins stiffened by fin rays and a more efficient gas exchange system in the gills.

  Class Cephalaspidomorphi: Lampreys are the oldest living lineage of vertebrates.

• Like hagfishes, lampreys offer clues to early chordate evolution but also have acquired unique characters.
• There are about 35 species of lampreys inhabiting both marine and freshwater environments.
  • Most lampreys are parasites that feed by clamping a round, jawless mouth onto a fish.
  • They use their rasping tongues to penetrate the skin of their fish prey and to ingest the prey’s blood.
• Lampreys live as suspension-feeding larvae in streams for years before migrating to the sea or lakes as adults.
  • These larvae resemble lancelets and live partially buried in sediment.
• Some species of lampreys feed only as larvae.
  • After metamorphosis, these lampreys attain sexual maturity, reproduce, and die within a few days.
• The skeletons of lampreys are made of cartilage.
  • Unlike most vertebrate cartilage, lamprey cartilage contains no collagen. Instead, it is a stiff protein matrix.
• The notochord persists as the main axial skeleton in adult lampreys.
  • Lampreys also have a cartilaginous pipe surrounding the rodlike notochord.
  • Pairs of cartilaginous projections extend dorsally, partially enclosing the nerve cord with what might be a vestige of an early-stage vertebral column.

  Many vertebrate lineages emerged early.

• Conodonts were slender, soft-bodied vertebrates with prominent eyes.
  • At the anterior end of their mouth, they had a set of barbed hooks made of mineralized dental tissue.
• Conodonts ranged in length from 3 to 30 cm.
  • They probably hunted with their large eyes and impaled their prey on hooks.
  • The food then passed to the pharynx, where a different set of dental elements crushed and sliced it.
• Conodonts were very abundant for more than 300 million years.
• Other vertebrates emerged during the Ordovician and Silurian periods.
  • These vertebrates had paired fins and an inner ear with two semicircular canals that provided a sense of balance.
• Although they lacked jaws, they had a muscular pharynx that may have sucked in detritus or bottom-dwelling organisms.
• They were armored with mineralized bone that offered protection from predators.
• The vertebrate skeleton evolved initially as a structure of unmineralized cartilage.
  • Its mineralization began only after lampreys diverged from other vertebrates.
• What initiated the process of mineralization in vertebrates?
  • Mineralization may have been associated with the transition to new feeding mechanisms.
• The earliest known mineralized structures in vertebrates were conodont dental elements.
• The armor seen in later jawless vertebrates was derived from dental mineralization.
  • Only in more derived vertebrates did the endoskeleton begin to mineralize, starting with the skull.

Concept 34.4 Gnathostomes are vertebrates that have jaws

• The gnathostomes have true jaws, hinged structures that enable vertebrates to grasp food firmly.
  • According to one hypothesis, gnathostome jaws evolved by modification of the skeletal rods that had previously supported the anterior pharyngeal gill slits.
  • The remaining gill slits were no longer required for suspension feeding and remained as the major sites of respiratory gas exchange.

  Gnathostomes have a number of shared, derived characters.

• Gnathostomes share other derived characters besides jaws.
• The common ancestors of all gnathostomes underwent an additional duplication of the Hox genes, so that the single cluster present in early chordates became four.
  • Other gene clusters also duplicated, allowing further complexity in the development of gnathostome embryos.
• The gnathostome forebrain is enlarged, in association with enhanced senses of vision and smell.
• The lateral line system evolved as a row of microscopic organs sensitive to vibrations in the surrounding water.
• The common ancestor of living gnathostomes had a mineralized axial skeleton, shoulder girdle, and two sets of paired appendages.
• Gnathostomes appeared in the fossil record in the mid-Ordovician period, about 470 million years ago, and steadily diversified.
• Gnathostome jaws and paired fins were major evolutionary breakthroughs.
  • Jaws, with the help of teeth, enable the animal to grip food items firmly and slice them up.
  • Paired fins, along with the tail, enable fishes to maneuver accurately while swimming.
• With these adaptations, many fish species were active predators, allowing for the diversification of both lifestyles and nutrient sources.
• The earliest gnathostomes in the fossil record are an extinct lineage of armored vertebrates called placoderms.
  • Most placoderms were less than a meter long, although some giants were more than 10 m long.
• Another group of jawed vertebrates called acanthodians radiated in the Devonian.
• Acanthodians were closely related to the ancestors of osteichthyans (ray-finned and lobe-finned fishes).
• Both placoderms and acanthodians disappeared by the beginning of the Carboniferous period, 360 million years ago.

  Class Chondrichthyes: Sharks and rays have cartilaginous skeletons.

• The class Chondrichthyes, sharks and their relatives, includes some of the biggest and most successful vertebrate predators in the oceans.
• Chondrichthyes have relatively flexible endoskeletons of cartilage rather than bone.
  • In most species, parts of the skeleton are impregnated by calcium.
• Conodonts and armored, jawless fishes show that mineralization of the vertebrate skeleton had begun before the chondrichthyan lineage branched off from other vertebrates.
  • Traces of bone can be found in living chondrichthyes, in their scales, at the base of their teeth and (in some sharks) in a thin layer on the surface of their vertebrae.
  • The loss of bone in chondrichthyes is a derived condition, which emerged after they diverged from other gnathostomes.
• There are about 750 extant species, almost all in the subclass of sharks and rays, with a few dozen species in a second subclass of chimaeras or ratfishes.
  • All have well-developed jaws and paired fins.
• The streamlined bodies of most sharks enable them to be swift, but not maneuverable, swimmers.
  • Powerful axial muscles power undulations of the body and caudal fin to drive the fish forward.
  • The dorsal fins provide stabilization.
  • While some buoyancy is provided by low-density oils in the large liver, the flow of water over the pectoral and pelvic fins also provides lift to keep the animal suspended in the water column.
• Continual swimming also ensures that water flows into the mouth and out through the gills.
  • Some sharks and many skates and rays spend much time resting on the seafloor, using the muscles of their jaws and pharynx to pump water over the gills.
• Most sharks 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 contrast, the largest sharks and rays are suspension feeders that consume plankton.
  • Sharks have several rows of teeth that gradually move to the front of the mouth as old teeth are lost.
  • Within the intestine of a shark is a spiral valve, a corkscrew-shaped ridge that increases surface area and prolongs the passage of food along the short digestive tract.
• Acute senses are adaptations that go along with the active, carnivorous lifestyle of sharks.
  • Sharks have sharp vision but cannot distinguish colors.
  • Their acute olfactory sense (smelling) occurs in a pair of nostrils that do not function in breathing.
  • Sharks can detect electrical fields, including those generated by the muscle contractions of nearby prey, through patches of specialized skin pores.
  • The lateral line system, a row of microscopic organs sensitive to pressure changes, can detect low-frequency vibrations.
  • In sharks, the whole body transmits sound to the hearing organs of the inner ear.
• Shark eggs are fertilized internally.
  • Males transfer sperm via claspers on their pelvic fins to the reproductive tract of the female.
  • Oviparous sharks encase their eggs in protective cases and lay them outside the mother’s body.
    • These hatch months later as juveniles.
  • Ovoviviparous sharks retain fertilized eggs in the oviduct.
    • The embryo completes development in the uterus, nourished by the egg yolk.
  • A few sharks are viviparous, providing nutrients through a placenta to the developing offspring.
• Rays are closely related to sharks, but they have adopted a very different lifestyle.
  • Most rays are flattened bottom dwellers that crush molluscs and crustaceans in their jaws.
  • The enlarged pectoral fins of rays are used like wings to propel the animal through the water.
  • The tail of many rays is whiplike and may bear venomous barbs for defense against threats.
• Chondrichthyans have changed little in more than 300 million years.
  • They are severely threatened by overfishing.
  • In 2003, researchers reported that shark stocks in the northwest Atlantic declined 75% in 15 years.

  Osteichthyes: The extant classes of bony fishes are the ray-finned fishes, the lobe-finned fishes, and the lungfishes.

• The vast majority of bony fishes belong to a clade of gnathostomes called the Osteichthyes (meaning “bony fish”).
• Systematists today include tetrapods with bony fish in Osteichthyes, which otherwise would be paraphyletic.
• Nearly all bony fishes have an ossified endoskeleton with a hard matrix of calcium phosphate.
  • It is not clear when the shift to a bony skeleton took place during gnathostome evolution.
• Bony fishes breathe by drawing water over four or five pairs of gills located in chambers covered by a protective flap, the operculum.
  • Water is drawn into the mouth, through the pharynx, and out between the gills by movements of the operculum and muscles surrounding the gill chambers.
• Most fishes have an internal, air-filled sac, the swim bladder.
  • The positive buoyancy provided by air counters the negative buoyancy of the tissues, enabling many fishes to be neutrally buoyant and remain suspended in the water.
  • The swim bladder evolved from balloonlike lungs that may have been used to breathe air when dissolved oxygen levels were low in stagnant shallow waters.
• The skin of bony fishes is often covered with thin, flattened bony scales that differ in structure from the toothlike scales of sharks.
• Glands in the skin secrete mucus that reduces drag in swimming.
• Like sharks, aquatic osteichthyes have a lateral line system, which is evident as a row of tiny pits in the skin on either side of the body.
• The reproduction of aquatic osteichthyes varies.
  • Most species are oviparous, reproducing by external fertilization after the female sheds large numbers of small eggs.
  • Internal fertilization and birthing characterize other species.
• The most familiar families of fishes belong to the ray-finned fishes, members of class Actinopterygii.
  • This class includes bass, trout, perch, tuna, and herring.
  • In this group, the fins are supported by long, flexible rays.
  • The fins may be modified for maneuvering, defense, and other functions.
• Bony fishes, including the ray-finned fishes, probably evolved in fresh water and then spread to the seas during their long history.
  • Many species of ray-finned fishes returned to fresh water at some point in their evolution.
  • Some ray-finned fishes, such as salmon, make a round-trip from fresh water to seawater and back to fresh water during their life cycle.
• Ray-finned fishes evolved during the Devonian period, along with the lobe-finned fishes (Sarcopterygii).
• The key derived character in lobe-fins is the presence of muscular pectoral and pelvic fins supported by extensions of the bony skeleton.
  • Many Devonian lobe-fins were large, bottom dwellers that may have used their paired, muscular fins to “walk” along the bottom.
  • By the end of the Devonian period, lobe-fin diversity was dwindling.
• Today, only three lineages survive.
  • One lineage, the coelacanths (class Actinistia) probably originated as freshwater animals with lungs, but others shifted to the ocean, including the only living genus, Latimeria.
  • The second lineage of living lobe-fins is represented by three genera of lungfishes (class Dipnoi), which live today in the Southern Hemisphere.
    • They generally inhabit stagnant ponds and swamps.
    • They can gulp air into lungs connected to the pharynx of the digestive tract to provide oxygen for metabolism.
    • 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.
  • The third lineage of lobe-fins that survives today is far more diverse than coelacanths or lungfishes.
• During the mid-Devonian, the tetrapods adapted to life on land and gave rise to terrestrial vertebrates, including humans.

Concept 34.5 Tetrapods are gnathostomes that have limbs and feet

• One of the most significant events in vertebrate history took place 360 million years ago, when the fins of some lobe-fins evolved into tetrapod limbs and feet.
• The most significant character of tetrapods is the four limbs, which allow them to support their weight on land.
  • The feet of tetrapods have digits that allow them to transmit muscle-generated forces to the ground when they walk.
• With the move to land, the bones of the pelvic girdle (to which the hind legs are attached) became fused to the backbone, permitting forces generated by the hind legs against the ground to be transferred to the rest of the body.
• Living tetrapods do not have pharyngeal gill slits.
  • The ears are adapted to the detection of airborne sounds.
• The Devonian coastal wetlands were home to a wide range of lobe-fins. Those that entered shallow, oxygen-poor water could use their lungs to breathe air.
• Some species likely used their stout fins to move across the muddy bottom.
  • At the water’s edge, leglike appendages were probably better equipment than fins for paddling and crawling through the dense vegetation in shallow water.
  • The tetrapod body plan was thus a modification of a preexisting body plan.
• In one lineage of lobe-fins, the fins became progressively more limb-like, while the rest of the body retained adaptations for aquatic life.
  • For example, fossils of Acanthostega from 365 million years ago had bony gill supports and rays in its tail to support propulsion in water, but it also had fully formed legs, ankles, and digits.
  • Acanthostega is representative of a period of vertebrate evolution when adaptations for shallow water allowed certain fishes to make a gradual transition to the terrestrial side of the water’s edge.
• A great diversity of tetrapods emerged during the Carboniferous period.
  • Judging from the morphology and location of the fossils, most of these early tetrapods remained tied to water.

  Class Amphibia: Salamanders, frogs, and caecilians are the three extant amphibian orders.

• Today the amphibians (class Amphibia) are represented by about 4,800 species of salamanders (order Urodela, “tailed ones”), frogs (order Anura, “tail-less ones”), and caecilians (order Apoda, “legless ones”).
• Some of the 500 species of urodeles are entirely aquatic, but others live on land as adults or throughout life.
  • On land, most salamanders walk with a side-to-side bending of the body that may resemble the swagger of the early terrestrial tetrapods.
• The 4,200 species of anurans are more specialized than urodeles for moving on land.
  • Adult frogs use powerful legs to hop along the terrain.
  • Frogs nab insects by flicking out their sticky tongues, which are attached to the front of the mouth.
• Anurans may be camouflaged or secrete a distasteful, even poisonous, mucus from skin glands.
  • Many poisonous species are brightly colored, perhaps to warn predators who associate the coloration with danger.
• Apodans, the caecilians (about 150 species), are legless and nearly blind.
  • The reduction of legs evolved secondarily from a legged ancestor.
• Superficially resembling earthworms, most species burrow in moist forest soil in the tropics.
  • A few South American species live in freshwater ponds and streams.
• Amphibian means “two lives,” a reference to the metamorphosis of many frogs from an aquatic stage, the tadpole, to the terrestrial adult.
  • Tadpoles are usually aquatic herbivores with gills and a lateral line system, and they swim by undulating their tails.
  • During metamorphosis, the tadpole develops legs, the lateral line disappears, and lungs replace gills.
  • Adult frogs are carnivorous hunters.
• Many amphibians do not live a dualistic—aquatic and terrestrial—life.
  • There are some strictly aquatic, and some strictly terrestrial frogs, salamanders, and caecilians.
  • The larvae of salamanders and caecilians look like adults and are also carnivorous.
• Paedomorphosis, the retention of some larval features in a sexually mature adult, is common among some groups of salamanders.
  • For example, the mudpuppy (Necturus) retains gills and other larval features when sexually mature.
• Most amphibians retain close ties with water and are most abundant in damp habitats.
  • Those adapted to drier habitats spend much of their time in burrows or under moist leaves where the humidity is higher.
  • Most amphibians rely heavily on their moist skin to carry out gas exchange with the environment.
    • Some terrestrial species lack lungs entirely and breathe exclusively through their skin and oral cavity.
• Amphibian eggs lack a shell and dehydrate quickly in dry air.
  • Most species have external fertilization, with eggs shed in ponds or swamps or at least in moist environments.
  • Some species lay vast numbers of eggs in temporary pools where mortality is high.
  • Others display various types of parental care and lay relatively few eggs.
    • In some species, males or females may house eggs on the back, in the mouth, or even in the stomach.
    • Some species are ovoviviparous or viviparous, retaining the developing eggs in the female reproductive tract until released as juveniles.
• Many amphibians display complex and diverse social behavior, especially during the breeding season.
  • Then many male frogs fill the air with their mating calls as they defend breeding territories or attract females.
  • In some terrestrial species, migrations to specific breeding sites may involve vocal communication, celestial navigation, or chemical signaling.
• For the past 25 years, zoologists have been documenting a rapid and alarming decline in amphibian populations throughout the world.
• Several causes that have been proposed include habitat degradation, the spread of a pathogen (a chytrid fungus), and acid precipitation.
  • Acid precipitation is damaging to amphibians because of their dependence on wet places for completion of their life cycles.

Concept 34.6 Amniotes are tetrapods that have a terrestrially adapted egg

• The amniote clade consists of the mammals and reptiles (including birds).
• The evolution of amniotes from an amphibian ancestor involved many adaptations for terrestrial living.
• The amniotic egg is the major derived character of the clade.
• Inside the shell of the amniotic egg are several extraembryonic membranes that function in gas exchange, waste storage, and the transfer of stored nutrients to the embryo.
  • The amniotic egg is named for one of these membranes, the amnion, which encloses a fluid-filled “private pond” that bathes the embryo and acts as a hydraulic shock absorber.
• The amniotic eggs enabled terrestrial vertebrates to complete their life cycles entirely on land.
  • In contrast to the shell-less eggs of amphibians, the amniotic eggs of most amniotes have a shell that retains water and can be laid in a dry place.
  • The calcareous shells of bird eggs are inflexible, while the leathery eggs of many reptiles are flexible.
  • Most mammals have dispensed with the shell.
    • The embryo implants in the wall of the uterus and obtains its nutrition from the mother.
• Amniotes acquired other adaptations to terrestrial life, including less-permeable skin and the increasing use of the rib cage to ventilate the lungs.
• Amniotes adopt a more elevated stance than earlier tetrapods and living amphibians.
• The most recent common ancestor of living amphibians and amniotes lived about 340 million years ago, in the early Carboniferous period.
  • No fossils of amniotic eggs have been found from that time.
• Early amniotes lived in drier environments than did earlier tetrapods.
• Some were herbivores, with grinding teeth. Others were large and predatory.

  The reptile clade includes birds.

• The reptile clade includes tuatara, lizards, snakes, turtles, crocodilians, and birds, as well as extinct groups such as dinosaurs.
• Reptiles have several adaptations for terrestrial life not generally found in amphibians.
  • Scales containing the protein keratin waterproof the skin, preventing dehydration in dry air.
    • Crocodiles, which are adapted to water, have evolved more permeable scales called scutes.
  • Reptiles obtain all their oxygen with lungs, not through their dry skin.
    • As an exception, many turtles can use the moist surfaces of their cloaca for gas exchange.
• Most reptiles lay shelled amniotic eggs on land.
  • Fertilization occurs internally, before the shell is secreted as the egg passes through the female’s reproductive tract.
  • Some species of lizards and snakes are viviparous, with their extraembryonic membranes forming a placenta that enables the embryo to obtain nutrients from its mother.
• Nonbird reptiles are sometimes labeled “cold-blooded” because they do not use their metabolism extensively to control body temperature.
  • However, many nonbird reptiles regulate their body temperature behaviorally by basking in the sun when cool and seeking shade when hot.
• Because they absorb external heat rather than generating much of their own, nonbird reptiles are more appropriately called ectotherms.
  • One advantage of this strategy is that an ectothermic reptile can survive on less than 10% of the calories required by a mammal of equivalent size.
• The reptile clade is not entirely ectothermic.
  • Birds are endothermic, capable of keeping the body warm through metabolism.
• The oldest reptilian fossils date back to the Carboniferous period, about 300 million years ago.
• The first major group of reptiles to emerge was the parareptiles, large, stocky, quadrupedal herbivores.
  • Some parareptiles had dermal plates on their skin, which may have provided defense against predators.
• Parareptiles died out 200 million years ago, at the end of the Triassic period.
• As parareptiles were dwindling, an equally ancient clade of reptiles, the diapsids, was diversifying.
  • The most obvious derived character of diapsids is a pair of holes on each side of the skull, behind the eye socket.
• The diapsids are composed of two main lineages.
  • One, the lepidosaurs, includes lizards, snakes, and tuataras.
    • This lineage also produced a number of marine reptiles including plesiosaurs and ichthyosaurs.
  • The archosaurs include crocodilians, and the extinct pterosaurs and dinosaurs.
• Pterosaurs, which originated in the late Triassic, were the first flying tetrapods.
  • The pterosaur wing is formed from a bristle-covered membrane of skin that stretched between the hind leg and the tip of an elongated finger.
  • Well-preserved fossils show the presence of muscles, blood vessels, and nerves in the wing membrane, suggesting that pterosaurs could dynamically adjust their membranes to assist their flight.
• Dinosaurs were an extremely diverse group varying in body shape, size, and habitat.
  • There were two main dinosaur lineages: the ornithischians, which were mostly herbivorous, and the saurischians, which included both long-necked giant herbivores and bipedal carnivorous theropods.
    • Theropods included the famous Tyrannosaurus rex as well as the ancestors of birds.
• There is increasing evidence that many dinosaurs were agile; fast moving; and, in some species, social.
  • Paleontologists have discovered signs of parental care among dinosaurs.
• There is continuing debate about whether dinosaurs were endothermic, capable of keeping their body warm through metabolism.
  • Some experts are skeptical.
  • In the warm, consistent Mesozoic climate, behavioral adaptations may have been sufficient for maintaining a suitable body temperature for terrestrial dinosaurs.
  • Also, the low surface-to-volume ratios would have reduced the effects of daily fluctuations in air temperature on the animal’s internal temperature.
  • Some anatomical evidence supports the hypothesis that at least some dinosaurs were endotherms.
    • Paleontologists have found fossils of dinosaurs in both Antarctica and the Arctic, although the climate in those areas was milder during the Mesozoic than today.
  • The dinosaur that gave rise to birds was certainly endothermic, as are all birds.
• By the end of the Cretaceous, all dinosaurs (except birds) became extinct.
  • It is uncertain whether dinosaurs were declining before they were finished off by an asteroid or comet impact.
• Lepidosaurs are represented by two living lineages.
• One lineage includes the tuatara, two species of lizard-like reptiles found only on 30 islands off the coast of New Zealand.
  • Tuatara relatives lived at least 220 million years ago, when they thrived on every continent well into the Cretaceous period.
• The other major living lineage of lepidosaurs are the squamates (lizards and snakes).
• Lizards are the most numerous and diverse reptiles alive today.
  • Most are relatively small, but they range in length from 16 mm to 3 m.
• Snakes are legless lepidosaurs that evolved from lizards closely related to the Komodo dragon.
• It was once thought that snakes were descendents of lizards that adapted to a burrowing lifestyle through the loss of limbs.
  • However, recently discovered fossils of aquatic snakes with complete hind legs suggest that snakes likely evolved in water and then recolonized land.
  • Some species of snakes retain vestigial pelvic and limb bones, providing evidence of their ancestry.
• Snakes are carnivorous, and a number of adaptations aid them in hunting and eating prey.
  • Snakes have acute chemical sensors and are sensitive to ground vibrations.
    • The flicking tongue fans odors toward olfactory organs on the roof of the mouth.
  • Heat-detecting organs of pit vipers, including rattlesnakes, enable these night hunters to locate warm animals.
  • Some poisonous snakes inject their venom through a pair of sharp, hollow or grooved teeth.
  • Loosely articulated jaws enable most snakes to swallow prey larger than the diameter of the snake itself.
• Turtles are the most distinctive group of reptiles alive today.
• All turtles have a boxlike shell made up of upper and lower shields that are fused to the vertebrae, clavicles, and ribs.
• The earliest fossils of turtles are 220 million years old, with fully developed shells.
  • The origin of the turtle shell remains a puzzle.
    • Some paleontologists suggest that turtle shells evolved from the dermal shells of parareptiles.
  • Other studies link turtles to archosaurs or lepidosaurs.
  • There are two separate branches of turtles that have independently evolved mechanisms to retract their heads.
  • Turtles live in a variety of environments, from deserts to ponds to the sea.
• Crocodiles and alligators (crocodilians) are among the largest living reptiles.
  • They spend most of their time in water, breathing air through upturned nostrils.
  • Crocodilians are confined to the tropics and subtropics.

  Birds evolved as feathered dinosaurs.

• Like crocodilians, birds are archosaurs, but highly specialized for flight.
  • In addition to amniotic eggs and scales, modern birds have feathers and other distinctive flight equipment.
• Almost every part of a typical bird’s anatomy is modified in some way to reduce weight and enhance flight.
  • One adaptation to reduce weight is the absence of some organs.
    • For instance, females have only one ovary.
  • Modern birds are toothless and grind their food in a muscular gizzard near the stomach.
• The skeletons of birds have several adaptations that make them light and flexible, but strong.
  • The bones are air-filled and honeycombed to reduce weight without sacrificing much strength.
• A bird’s feathers have a hollow, air-filled shaft that is light and strong.
  • Feathers are made of beta-keratin, a protein similar to the keratin of reptile scales.
• The shape and arrangement of feathers forms wings into airfoils.
• Power for flapping the wings comes from contractions of the pectoral muscles, anchored to a keel on the sternum.
• The evolution of flight required radical alteration in body form but provides many benefits.
  • Flight enhances hunting and scavenging.
    • It enables many birds to exploit flying insects, an abundant, highly nutritious food resource.
  • Flight provides a ready escape from earthbound predators.
  • It enables many birds to migrate great distances to exploit different food resources and seasonal breeding areas.
• Flying requires a great expenditure of energy with an active metabolism.
  • Birds are endothermic, using their own metabolic heat to maintain a constant body temperature.
    • Feathers and, in some species, a layer of fat provide insulation.
  • Efficient respiratory and circulatory systems with a four-chambered heart keep tissues well supplied with oxygen and nutrients.
    • The lungs have tiny tubes leading to and from elastic air sacs that help dissipate heat and reduce body density.
  • Birds have excellent vision and coordination, supported by well-developed areas of the brain.
    • The large brains of birds (proportionately larger than those of reptiles or amphibians) support very complex behavior.
  • During the breeding season, birds engage in elaborate courtship rituals.
    • This culminates in copulation, contact between the mates’ vents, the openings to their cloacae.
    • After eggs are laid, the avian embryo is kept warm through brooding by the mother, father, or both, depending on the species.
• Cladistic analyses of fossilized skeletons support the hypothesis that the closest reptilian ancestors of birds were theropods.
• In the late 1990s, Chinese paleontologists unearthed a treasure trove of feathered theropods that are shedding light on bird origins.
  • These fossils suggest that feathers evolved long before feathered flight, possibly for insulation or courtship.
• Theropods may have evolved powered flight by one of two possible routes.
  1. Small ground-running dinosaurs chasing prey or evading predation may have used feathers to gain extra lift as they jumped into the air.
  2. Dinosaurs could have glided from trees, aided by feathers.
• The most famous Mesozoic bird is Archaeopteryx, known from fossils from a German limestone quarry.
  • This ancient bird lived about 150 million years ago, during the late Jurassic period.
  • Archaeopteryx had clawed forelimbs, teeth, and a long tail containing vertebrae.
    • Without its feathers, Archaeopteryx would probably be classified as a theropod dinosaur.
    • Its skeletal anatomy indicates that it was a weak flyer, perhaps a tree-dwelling glider.
• Neornithes, the clade that includes 28 orders of living birds, arose after the Cretaceous-Tertiary boundary, 65 million years ago.
• Most birds can fly, but Neornithes includes a few flightless birds, the ratites, which lack both a breastbone and large pectoral muscles.
  • The ratites include the ostrich, kiwi, and emu.
• The penguins make up the flightless order Sphenisciformes.
  • They have powerful pectoral muscles, which they use in swimming.
• The demands of flight have rendered the general form of all flying birds similar to one another.
  • The beak of birds is very adaptable, taking on a great variety of shapes for different diets.

Concept 34.7 Mammals are amniotes that have hair and produce milk

Mammals diversified extensively in the wake of the Cretaceous extinctions.

• Mammals have a number of derived traits.
  • All mammalian mothers use mammary glands to nourish their babies with milk, a balanced diet rich in fats, sugars, proteins, minerals, and vitamins.
  • All mammals also have hair, made of keratin.
    • Hair and a layer of fat under the skin retain metabolic heat, contributing to endothermy in mammals.
  • Endothermy is supported by an active metabolism, made possible by efficient respiration and circulation.
    • Adaptations include a muscular diaphragm and a four-chambered heart.
• Mammals generally have larger brains than other vertebrates of equivalent size.
  • Many species are capable of learning.
  • The relatively long period of parental care extends the time for offspring to learn important survival skills by observing their parents.
• Feeding adaptations of the jaws and teeth are other important mammalian traits.
  • Unlike the uniform conical teeth of most reptiles, the teeth of mammals come in a variety of shapes and sizes adapted for processing many kinds of foods.
  • During the evolution of mammals from reptiles, two bones formerly in the jaw joint were incorporated into the mammalian ear and the jaw joint was remodeled.
• Mammals belong to a group of amniotes known as synapsids.
  • Synapsids have a temporal fenestra behind the eye socket on each side of the skull.
• Synapsids evolved into large herbivores and carnivores during the Permian period.
• Mammal-like synapsids emerged by the end of the Triassic, 200 million years ago.
  • These animals were not mammals, but they were small and likely hairy, fed on insects at night, and had a higher metabolism that other synapsids.
  • They likely laid eggs.
• The first true mammals arose in the Jurassic periods.
  • Early mammals diversified into a number of lineages, all about the size of a shrew.
• During the Mesozoic, mammals coexisted with dinosaurs and underwent a great adaptive radiation in the Cenozoic in the wake of the Cretaceous extinctions.
  • Modern mammals are split into three groups: monotremes (egg-laying mammals), marsupials (mammals with pouches), and eutherian (placental) mammals.
• Monotremes—the platypuses and the echidnas—are the only living mammals that lay eggs.
  • The reptile-like egg contains enough yolk to nourish the developing embryo.
• Monotremes have hair, and females produce milk in specialized glands.
  • After hatching, the baby sucks milk from the mother’s fur because she lacks nipples.
• Marsupials include opossums, kangaroos, bandicoots, and koalas.
• In contrast to monotremes, marsupials have a higher metabolic rate, have nipples that produce milk, and give birth to live young.
• A marsupial is born very early in development and, in most species, completes its embryonic development while nursing within a maternal pouch, the marsupium.
  • In most species, the tiny offspring climbs from the exit of the female’s reproductive tract to the mother’s pouch.
• Marsupials existed worldwide throughout the Mesozoic area but now are restricted to Australia and the Americas.
  • In Australia, marsupials have radiated and filled niches occupied by eutherian mammals in other parts of the world.
    • Through convergent evolution, these diverse marsupials resemble eutherian mammals that occupy similar ecological roles.
• While marsupial mammals diversified throughout the Tertiary in South America and Australia, the placental mammals began an adaptive radiation on the northern continents.
  • Australia’s isolation facilitated the diversification and survival of its marsupial fauna.
  • Invasions of placental mammals from North America impacted the marsupial fauna of South America about 12 million years ago and then again about 3 million years ago when the continents were connected by the Isthmus of Panama.
    • This mammalian biogeography is an example of the interplay between biological and geological evolution.
• Compared to marsupials, eutherian mammals (placentals) have a longer period of pregnancy.
  • Young eutherians complete their embryonic development within the uterus, joined to the mother by the placenta.
  • Eutherians are commonly called placental mammals because their placentas are more complex than those of marsupials and provide a more intimate and long-lasting association between mother and young.

Concept 34.8 Humans are bipedal hominoids with a large brain

Primate evolution provides a context for understanding human origins.

• Primates include lemurs, monkeys, and apes.
• Primates have large brains and short jaws.
• Their eyes are forward-looking.
• Most primates have hands and feet adapted for grasping.
• Relative to other mammals, they have large brains and short jaws.
• They have flat nails on their digits, rather than narrow claws.
• Primates also have relatively well-developed parental care and relatively complex social behavior.
• The earliest primates were probably tree dwellers, shaped by natural selection for arboreal life.
  • The grasping hands and feet of primates are adaptations for hanging on to tree branches.
    • All modern primates, except Homo, have a big toe that is widely separated from the other toes.
    • The thumb is relatively mobile and separate from the fingers in all primates, but a fully opposable thumb is found only in anthropoid primates.
    • The unique dexterity of humans, aided by distinctive bone structure at the thumb base, represents descent with modification from ancestral hands adapted for life in the trees.
• Other primate features also originated as adaptations for tree dwelling.
  • The overlapping fields of vision of the two eyes enhance depth perception, an obvious advantage when brachiating.
  • Excellent hand-eye coordination is also important for arboreal maneuvering.
• Primates are divided into two subgroups.
  • The Prosimii (prosimians) probably resemble early arboreal primates and include the lemurs of Madagascar and the lorises, pottos, and tarsiers of tropical Africa and southern Asia.
  • The Anthropoidea (anthropoids) include monkeys, apes, and humans.
• The oldest known anthropoid fossils, from about 45 million years ago, support the hypothesis that tarsiers are the prosimians most closely related to anthropoids.
• By the Oligocene, monkeys were established in Africa, Asia, and South America.
  • The Old World and New World monkeys underwent separate adaptive radiations.
  • All New World monkeys are arboreal, but Old World monkeys include arboreal and ground-dwelling species.
  • Most monkeys in both groups are diurnal, and usually live in bands held together by social behavior.
• In addition to monkeys, the anthropoid suborder also includes four genera of apes: Hylobates (gibbons), Pongo (orangutans), Gorilla (gorillas), and Pan (chimpanzees and bonobos).
  • Modern apes are confined exclusively to the tropical regions of the Old World.
  • They evolved from Old World monkeys about 20–25 million years ago.
• With the exception of gibbons, modern apes are larger than monkeys, with relatively long arms and short legs and no tails.
  • Only gibbons and orangutans are primarily arboreal.
• Social organization varies among the genera, with gorillas and chimpanzees being highly social.
  • Apes have relatively larger brains than monkeys, and their behavior is more flexible.

  Humans are bipedal hominoids.

• In the continuity of life spanning more than 3.5 billion years, humans and apes have shared ancestry for all but the past few million years.
• Human evolution is marked by the evolution of several major features.
  • Humans stand upright and walk on two legs.
  • Humans have a much larger brain than other hominoids and are capable of language, symbolic thought, and tool use.
  • Humans have reduced jawbones and muscles and a shorter digestive tract.
  • Human and chimpanzee genomes are 99% identical.
    • Scientists are comparing the genomes of humans and chimpanzees to investigate the 1% difference.
• Paleoanthropology is the study of human origins and evolution.
• Paleoanthropologists have found fossils of 20 species of extinct hominoids that are more closely related to humans than to chimpanzees.
  • These species are known as hominids.
• The oldest hominid is Sahelanthropus tchandensis, which lived 7 million years ago.
  • Sahelanthropus and other early hominids shared some of the derived characters of humans.
  • They had reduced canine teeth and relatively flat faces.
  • They were more upright and bipedal than other hominoids.
• While early hominids were becoming bipedal, their brains remained small—about 400 to 450 cm3 in volume.
  • Early hominids were small in stature, with relatively large teeth and a protruding lower jaw.
• Avoid three common sources of confusion:
  1. First, our ancestors were not chimpanzees or any other modern apes.
     • Chimpanzees and humans represent two divergent branches of the hominoid tree that evolved from a common ancestor that was neither a chimpanzee nor a human.
  2. Second, human evolution did not occur as a ladder with a series of steps leading directly from an ancestral hominoid to Homo sapiens.
     • If human evolution is a parade, then many splinter groups traveled down dead ends, and several different human species coexisted.
     • Human phylogeny is more like a multibranched bush with our species as the tip of the only surviving twig.
  3. Third, the various human characteristics, such as upright posture and an enlarged brain, did not evolve in unison.
  4. Different features evolved at different rates, called mosaic evolution.
  5. Our pedigree includes ancestors who walked upright but had brains much less developed than ours.
• After dismissing some of the folklore on human evolution, we must admit that many questions about our own ancestry remain.
• Hominid diversity increased dramatically between 4 and 2 million years ago.