The Origin and Evolution of Vertebrates Chapter 34 The Origin and Evolution of Vertebrates

Overview: Half a Billion Years of Backbones Early in the Cambrian period, about 530 million years ago, an astonishing variety of invertebrate animals inhabited Earth’s oceans One type of animal gave rise to vertebrates, one of the most successful groups of animals The animals called vertebrates get their name from vertebrae, the series of bones that make up the backbone © 2011 Pearson Education, Inc.

Figure 34.1 Figure 34.1 What is the relationship of this ancient organism to humans? 3

One lineage of vertebrates colonized land 365 million years ago There are about 52,000 species of vertebrates, including the largest organisms ever to live on the Earth Vertebrates have great disparity, a wide range of differences within the group © 2011 Pearson Education, Inc.

Concept 34.1: Chordates have a notochord and a dorsal, hollow nerve cord Chordates (phylum Chordata) are bilaterian animals that belong to the clade of animals known as Deuterostomia Chordates comprise all vertebrates and two groups of invertebrates, the urochordates and cephalochordates © 2011 Pearson Education, Inc.

ANCESTRAL DEUTEROSTOME Cephalochordata Chordates Urochordata Notochord Figure 34.2 Echinodermata ANCESTRAL DEUTEROSTOME Cephalochordata Chordates Urochordata Notochord Myxini Common ancestor of chordates Craniates Petromyzontida Head Chondrichthyes Vertebrates Vertebral column Actinopterygii Gnathostomes Jaws, mineralized skeleton Actinistia Osteichthyans Lungs or lung derivatives Lobe-fins Figure 34.2 Phylogeny of living chordates. Dipnoi Lobed fins Amphibia Tetrapods Reptilia Limbs with digits Amniotes Amniotic egg Mammalia Milk 6

ANCESTRAL DEUTEROSTOME Cephalochordata Figure 34.2a Echinodermata ANCESTRAL DEUTEROSTOME Cephalochordata Urochordata Notochord Myxini Common ancestor of chordates Petromyzontida Head Chondrichthyes Vertebral column Figure 34.2 Phylogeny of living chordates. Jaws, mineralized skeleton Osteichthyes 7

Lungs or lung derivatives Figure 34.2b Actinopterygii Actinistia Lungs or lung derivatives Dipnoi Lobed fins Amphibia Reptilia Limbs with digits Figure 34.2 Phylogeny of living chordates. Amniotic egg Mammalia Milk 8

Derived Characters of Chordates All chordates share a set of derived characters Some species have some of these traits only during embryonic development Four key characters of chordates Notochord Dorsal, hollow nerve cord Pharyngeal slits or clefts Muscular, post-anal tail © 2011 Pearson Education, Inc.

Dorsal, hollow nerve cord Muscle segments Figure 34.3 Dorsal, hollow nerve cord Muscle segments Notochord Mouth Figure 34.3 Chordate characteristics. Anus Pharyngeal slits or clefts Muscular, post-anal tail 10

Notochord The notochord is a longitudinal, flexible rod between the digestive tube and nerve cord It provides skeletal support throughout most of the length of a chordate In most vertebrates, a more complex, jointed skeleton develops, and the adult retains only remnants of the embryonic notochord © 2011 Pearson Education, Inc.

Dorsal, Hollow Nerve Cord The nerve cord of a chordate embryo develops from a plate of ectoderm that rolls into a tube dorsal to the notochord The nerve cord develops into the central nervous system: the brain and the spinal cord © 2011 Pearson Education, Inc.

Pharyngeal Slits or Clefts In most chordates, grooves in the pharynx called pharyngeal clefts develop into slits that open to the outside of the body Functions of pharyngeal slits Suspension-feeding structures in many invertebrate chordates Gas exchange in vertebrates (except vertebrates with limbs, the tetrapods) Develop into parts of the ear, head, and neck in tetrapods © 2011 Pearson Education, Inc.

Muscular, Post-Anal Tail Chordates have a tail posterior to the anus In many species, the tail is greatly reduced during embryonic development The tail contains skeletal elements and muscles It provides propelling force in many aquatic species © 2011 Pearson Education, Inc.

Lancelets Lancelets (Cephalochordata) are named for their bladelike shape They are marine suspension feeders that retain characteristics of the chordate body plan as adults © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN01 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN01 In-text art, p. 699 Amphibia Reptilia Mammalia 16

Dorsal, hollow nerve cord Figure 34.4 Cirri Mouth Pharyngeal slits Atrium Digestive tract Notochord Atriopore 1 cm Dorsal, hollow nerve cord Segmental muscles Figure 34.4 The lancelet Branchiostoma, a cephalochordate. Anus Tail 17

Dorsal, hollow nerve cord Figure 34.4a Cirri Mouth Pharyngeal slits Atrium Digestive tract Notochord Atriopore Dorsal, hollow nerve cord Segmental muscles Figure 34.4 The lancelet Branchiostoma, a cephalochordate. Anus Tail 18

Figure 34.4b Figure 34.4 The lancelet Branchiostoma, a cephalochordate. 1 cm 19

Tunicates Tunicates (Urochordata) are more closely related to other chordates than are lancelets Trunicates most resemble chordates during their larval stage, which may last only a few minutes As an adult, a tunicate draws in water through an incurrent siphon, filtering food particles When attacked, trunicates, or “sea squirts,” shoot water through their excurrent siphon © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN02 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN02 In-text art, p. 700 Amphibia Reptilia Mammalia 21

Dorsal, hollow nerve cord Pharynx with numerous slits Figure 34.5 Incurrent siphon to mouth Water flow Notochord Dorsal, hollow nerve cord Excurrent siphon Tail Excurrent siphon Excurrent siphon Atrium Incurrent siphon Muscle segments Pharynx with numerous slits Intestine Anus Stomach Intestine Tunic Atrium Figure 34.5 A tunicate, a urochordate. Esophagus Pharynx with slits Stomach (a) Tunicate larva (b) Adult tunicate (c) Adult tunicate 22

Dorsal, hollow nerve cord Pharynx with numerous slits Figure 34.5a Incurrent siphon to mouth Water flow Notochord Dorsal, hollow nerve cord Tail Excurrent siphon Excurrent siphon Atrium Incurrent siphon Muscle segments Pharynx with numerous slits Intestine Anus Stomach Intestine Figure 34.5 A tunicate, a urochordate. Tunic Atrium Esophagus Pharynx with slits Stomach (a) Tunicate larva (b) Adult tunicate 23

Pharynx with numerous slits Figure 34.5b Incurrent siphon to mouth Excurrent siphon Atrium Pharynx with numerous slits Figure 34.5 A tunicate, a urochordate. Tunic (c) Adult tunicate 24

Tunicates are highly derived and have fewer Hox genes than other vertebrates © 2011 Pearson Education, Inc.

Early Chordate Evolution Ancestral chordates may have resembled lancelets The same Hox genes that organize the vertebrate brain are expressed in the lancelet’s simple nerve cord tip Genome sequencing suggests that Genes associated with the heart and thyroid are common to all chordates Genes associated with transmission of nerve impulses are unique to vertebrates © 2011 Pearson Education, Inc.

Nerve cord of lancelet embryo Figure 34.6 BF1 Otx Hox3 Nerve cord of lancelet embryo BF1 Otx Hox3 Brain of vertebrate embryo (shown straightened) Figure 34.6 Expression of developmental genes in lancelets and vertebrates. Forebrain Midbrain Hindbrain 27

Concept 34.2: Craniates are chordates that have a head The origin of a head enabled chordates to coordinate more complex movement and feeding behaviors Craniates share some characteristics: a skull, brain, eyes, and other sensory organs © 2011 Pearson Education, Inc.

Derived Characters of Craniates Craniates have two clusters of Hox genes; lancelets and tunicates have only one cluster One feature unique to craniates is the neural crest, a collection of cells near the dorsal margins of the closing neural tube in an embryo Neural crest cells give rise to a variety of structures, including some of the bones and cartilage of the skull © 2011 Pearson Education, Inc.

Dorsal edges of neural plate Neural crest Neural tube Figure 34.7 Dorsal edges of neural plate Neural crest Neural tube Notochord Migrating neural crest cells (a) (b) (c) Skull bones and cartilage derived from neural crest cells Figure 34.7 The neural crest, embryonic source of many unique craniate characters. 30

In aquatic craniates the pharyngeal clefts evolved into gill slits Craniates have a higher metabolism and are more muscular than tunicates and lancelets Craniates have a heart with at least two chambers, red blood cells with hemoglobin, and kidneys © 2011 Pearson Education, Inc.

The Origin of Craniates Fossils from the Cambrian explosion document the transition to craniates The most primitive of the fossils are those of the 3-cm-long Haikouella Haikouella had a well-formed brain, eyes, and muscular segments, but not a skull © 2011 Pearson Education, Inc.

5 mm Segmented muscles Pharyngeal slits Figure 34.8 Figure 34.8 Fossil of an early chordate. Segmented muscles Pharyngeal slits 33

Figure 34.8a Figure 34.8 Fossil of an early chordate. 5 mm 34

Myllokunmingia had parts of a skull and was a true craniate In other Cambrian rocks, paleontologists have found fossils of even more advanced chordates, such as Myllokunmingia Myllokunmingia had parts of a skull and was a true craniate © 2011 Pearson Education, Inc.

Hagfishes The most basal group of craniates is Myxini, the hagfishes Hagfishes have a cartilaginous skull and axial rod of cartilage derived from the notochord, but lack jaws and vertebrae They have a small brain, eyes, ears, and tooth-like formations Hagfishes are marine; most are bottom-dwelling scavengers © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN03 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN03 In-text art, p. 702 Amphibia Reptilia Mammalia 37

Figure 34.9 Slime glands Figure 34.9 A hagfish. 38

Concept 34.3: Vertebrates are craniates that have a backbone During the Cambrian period, a lineage of craniates evolved into vertebrates Vertebrates became more efficient at capturing food and avoiding being eaten © 2011 Pearson Education, Inc.

Derived Characters of Vertebrates Vertebrates underwent a second gene duplication involving the Dlx family of transcription factors Vertebrates have the following derived characters Vertebrae enclosing a spinal cord An elaborate skull Fin rays, in the aquatic forms © 2011 Pearson Education, Inc.

Lampreys Lampreys (Petromyzontida) represent the oldest living lineage of vertebrates They are jawless vertebrates that feed by clamping their mouth onto a live fish They inhabit various marine and freshwater habitats They have cartilaginous segments surrounding the notochord and arching partly over the nerve cord © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN04 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN04 In-text art, p. 703 Amphibia Reptilia Mammalia 42

Figure 34.10 Figure 34.10 A sea lamprey. 43

Figure 34.10a Figure 34.10 A sea lamprey. 44

Figure 34.10b Figure 34.10 A sea lamprey. 45

Fossils of Early Vertebrates Conodonts were the first vertebrates with mineralized skeletal elements in their mouth and pharynx Their fossilized dental elements are common in the fossil record © 2011 Pearson Education, Inc.

Dental elements (within head) Figure 34.11 Dental elements (within head) Figure 34.11 A conodont. 47

Other armored, jawless vertebrates had defensive plates of bone on their skin © 2011 Pearson Education, Inc.

Pteraspis Pharyngolepis Figure 34.12 Figure 34.12 Jawless armored vertebrates. Pharyngolepis 49

Origins of Bone and Teeth Mineralization appears to have originated with vertebrate mouthparts The vertebrate endoskeleton became fully mineralized much later © 2011 Pearson Education, Inc.

Concept 34.4: Gnathostomes are vertebrates that have jaws Today, jawed vertebrates, or gnathostomes, outnumber jawless vertebrates Gnathostomes include sharks and their relatives, ray-finned fishes, lobe-finned fishes, amphibians, reptiles (including birds), and mammals © 2011 Pearson Education, Inc.

Derived Characters of Gnathostomes Gnathostomes have jaws that might have evolved from skeletal supports of the pharyngeal slits © 2011 Pearson Education, Inc.

Gill slits Cranium Mouth Skeletal rods Figure 34.13 Figure 34.13 Hypothesis for the evolution of vertebrate jaws. 53

Other characters common to gnathostomes Genome duplication, including duplication of Hox genes An enlarged forebrain associated with enhanced smell and vision In aquatic gnathostomes, the lateral line system, which is sensitive to vibrations © 2011 Pearson Education, Inc.

Fossil Gnathostomes The earliest gnathostomes in the fossil record are an extinct lineage of armored vertebrates called placoderms They appeared in the Ordovician, about 450 million years ago © 2011 Pearson Education, Inc.

Figure 34.14 0.5 m Figure 34.14 Fossil of an early gnathostome. 56

Another group of jawed vertebrates called acanthodians radiated during the Silurian and Devonian periods (444 to 359 million years ago) Three lineages of jawed vertebrates survive today: chondrichthyans, ray-finned fishes, and lobe-fins © 2011 Pearson Education, Inc.

Chondrichthyans (Sharks, Rays, and Their Relatives) Chondrichthyans (Chondrichthyes) have a skeleton composed primarily of cartilage The largest and most diverse group of chondrichthyans includes the sharks, rays, and skates © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN05 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN05 In-text art, p. 705 Amphibia Reptilia Mammalia 59

(a) Blacktip reef shark (Carcharhinus melanopterus) Figure 34.15 Dorsal fins Pectoral fins Pelvic fins (a) Blacktip reef shark (Carcharhinus melanopterus) (b) Southern stingray (Dasyatis americana) Figure 34.15 Chondrichthyans. (c) Spotted ratfish (Hydrolagus colliei) 60

(a) Blacktip reef shark (Carcharhinus melanopterus) Figure 34.15a Dorsal fins Pectoral fins Pelvic fins Figure 34.15 Chondrichthyans. (a) Blacktip reef shark (Carcharhinus melanopterus) 61

(b) Southern stingray (Dasyatis americana) Figure 34.15b Figure 34.15 Chondrichthyans. (b) Southern stingray (Dasyatis americana) 62

A second subclass is composed of a few dozen species of ratfishes © 2011 Pearson Education, Inc.

(c) Spotted ratfish (Hydrolagus colliei) Figure 34.15c Figure 34.15 Chondrichthyans. (c) Spotted ratfish (Hydrolagus colliei) 64

Sharks have a streamlined body and are swift swimmers The largest sharks are suspension feeders, but most are carnivores Sharks have a short digestive tract; a ridge called the spiral valve to increase the digestive surface area Sharks have acute senses including sight, smell, and the ability to detect electrical fields from nearby animals © 2011 Pearson Education, Inc.

Shark eggs are fertilized internally but embryos can develop in different ways Oviparous: Eggs hatch outside the mother’s body Ovoviviparous: The embryo develops within the uterus and is nourished by the egg yolk Viviparous: The embryo develops within the uterus and is nourished through a yolk sac placenta from the mother’s blood © 2011 Pearson Education, Inc.

The reproductive tract, excretory system, and digestive tract empty into a common cloaca © 2011 Pearson Education, Inc.

Ray-Finned Fishes and Lobe-Fins The vast majority of vertebrates belong to a clade of gnathostomes called Osteichthyes Nearly all living osteichthyans have a bony endoskeleton Osteichthyans includes the bony fish and tetrapods Aquatic osteichthyans are the vertebrates we informally call fishes © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN06 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN06 In-text art, p. 707 Amphibia Reptilia Mammalia 69

Fishes control their buoyancy with an air sac known as a swim bladder Most fishes breathe by drawing water over gills protected by an operculum Fishes control their buoyancy with an air sac known as a swim bladder Fishes have a lateral line system Most species are oviparous, but some have internal fertilization and birthing © 2011 Pearson Education, Inc.

Swim bladder Dorsal fin Caudal fin Spinal cord Adipose fin Brain Figure 34.16 Swim bladder Dorsal fin Caudal fin Spinal cord Adipose fin Brain Nostril Cut edge of operculum Anal fin Liver Anus Figure 34.16 Anatomy of a trout, a ray-finned fish. Lateral line Gills Gonad Stomach Kidney Pelvic fin Intestine Urinary bladder Heart 71

Ray-Finned Fishes Actinopterygii, the ray-finned fishes, includes nearly all the familiar aquatic osteichthyans Ray-finned fishes originated during the Silurian period (444 to 416 million years ago) The fins, supported mainly by long, flexible rays, are modified for maneuvering, defense, and other functions © 2011 Pearson Education, Inc.

Yellowfin tuna (Thunnus albacares) Figure 34.17 Yellowfin tuna (Thunnus albacares) Red lionfish (Pterois volitans) Common sea horse (Hippocampus ramulosus) Figure 34.17 Ray-finned fishes (Actinopterygii). Fine-spotted moray eel (Gymnothorax dovii) 73

Yellowfin tuna (Thunnus albacares) Figure 34.17a Yellowfin tuna (Thunnus albacares) Figure 34.17 Ray-finned fishes (Actinopterygii). 74

Red lionfish (Pterois volitans) Figure 34.17b Red lionfish (Pterois volitans) Figure 34.17 Ray-finned fishes (Actinopterygii). 75

Common sea horse (Hippocampus ramulosus) Figure 34.17c Common sea horse (Hippocampus ramulosus) Figure 34.17 Ray-finned fishes (Actinopterygii). 76

Fine-spotted moray eel (Gymnothorax dovii) Figure 34.17d Figure 34.17 Ray-finned fishes (Actinopterygii). Fine-spotted moray eel (Gymnothorax dovii) 77

Lobe-Fins The lobe-fins (Sarcopterygii) have muscular pelvic and pectoral fins Lobe-fins also originated in the Silurian period © 2011 Pearson Education, Inc.

5 cm Lower jaw Scaly covering Dorsal spine Figure 34.18 Figure 34.18 A reconstruction of an ancient lobe-fin. 79

5 cm Lower jaw Scaly covering Dorsal spine Figure 34.18a Figure 34.18 A reconstruction of an ancient lobe-fin. Lower jaw Scaly covering Dorsal spine 80

Three lineages survive and include coelacanths, lungfishes, and tetrapods Coelacanths were thought to have become extinct 75 million years ago, but a living coelacanth was caught off the coast of South Africa in 1938 © 2011 Pearson Education, Inc.

Figure 34.19 Figure 34.19 A coelacanth (Latimeria). 82

Concept 34.5: Tetrapods are gnathostomes that have limbs One of the most significant events in vertebrate history was when the fins of some lobe-fins evolved into the limbs and feet of tetrapods © 2011 Pearson Education, Inc.

Derived Characters of Tetrapods Tetrapods have some specific adaptations Four limbs, and feet with digits A neck, which allows separate movement of the head Fusion of the pelvic girdle to the backbone The absence of gills (except some aquatic species) Ears for detecting airborne sounds © 2011 Pearson Education, Inc.

The Origin of Tetrapods Tiktaalik, nicknamed a “fishapod,” shows both fish and tetrapod characteristics It had Fins, gills, lungs, and scales Ribs to breathe air and support its body A neck Fins with the bone pattern of a tetrapod limb © 2011 Pearson Education, Inc.

Fish Characters Tetrapod Characters Figure 34.20 Fish Characters Tetrapod Characters Scales Fins Gills and lungs Neck Ribs Fin skeleton Flat skull Eyes on top of skull Shoulder bones Ribs Neck Scales Head Eyes on top of skull Humerus Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. Ulna Flat skull “Wrist” Elbow Radius Fin Fin skeleton 86

Shoulder bones Neck Head Eyes on top of skull Flat skull Fin Figure 34.20a Shoulder bones Neck Head Eyes on top of skull Flat skull Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. Fin 87

Figure 34.20b Ribs Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. 88

Figure 34.20c Scales Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. 89

Humerus Ulna “Wrist” Elbow Radius Fin skeleton Figure 34.20d Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. Fin skeleton 90

Fish Characters Tetrapod Characters Figure 34.20e Fish Characters Tetrapod Characters Scales Fins Gills and lungs Neck Ribs Fin skeleton Flat skull Eyes on top of skull Figure 34.20 Impact: Discovery of a “Fishapod”: Tiktaalik. 91

Tiktaalik could most likely prop itself on its fins, but not walk The first tetrapods appeared 365 million years ago © 2011 Pearson Education, Inc.

Time (millions of years ago) Figure 34.21 Lungfishes Eusthenopteron Panderichthys Tiktaalik Acanthostega Tulerpeton Limbs with digits Figure 34.21 Steps in the origin of limbs with digits. Amphibians Key to limb bones Ulna Radius Amniotes Humerus Silurian PALEOZOIC Devonian Carboniferous Permian 415 400 385 370 355 340 325 310 295 280 265 Time (millions of years ago) 93

Lobe-fins with limbs with digits Key to limb bones Figure 34.21a Lungfishes Eusthenopteron Panderichthys Tiktaalik Lobe-fins with limbs with digits Figure 34.21 Steps in the origin of limbs with digits. Key to limb bones Ulna Silurian PALEOZOIC Radius Devonian Carboniferous Permian Humerus 415 400 385 370 355 340 325 310 295 280 265 Time (millions of years ago) 94

Time (millions of years ago) Figure 34.21b Acanthostega Tulerpeton Limbs with digits Amphibians Key to limb bones Ulna Radius Amniotes Humerus Figure 34.21 Steps in the origin of limbs with digits. Silurian PALEOZOIC Devonian Carboniferous Permian 415 400 385 370 355 340 325 310 295 280 265 Time (millions of years ago) 95

Amphibians Amphibians (class Amphibia) are represented by about 6,150 species Order Urodela includes salamanders, which have tails © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN07 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN07 In-text art, p. 710 Amphibia Reptilia Mammalia 97

(a) Order Urodela (salamanders) Figure 34.22 (a) Order Urodela (salamanders) (b) Order Anura (frogs) Figure 34.22 Amphibians. (c) Order Apoda (caecilians) 98

(a) Order Urodela (salamanders) Figure 34.22a Figure 34.22 Amphibians. (a) Order Urodela (salamanders) 99

Order Anura includes frogs and toads, which lack tails © 2011 Pearson Education, Inc.

(b) Order Anura (frogs) Figure 34.22b Figure 34.22 Amphibians. (b) Order Anura (frogs) 101

Order Apoda includes caecilians, which are legless and resemble worms © 2011 Pearson Education, Inc.

(c) Order Apoda (caecilians) Figure 34.22c Figure 34.22 Amphibians. (c) Order Apoda (caecilians) 103

Amphibian means “both ways of life,” referring to the metamorphosis of an aquatic larva into a terrestrial adult Most amphibians have moist skin that complements the lungs in gas exchange © 2011 Pearson Education, Inc.

(b) During metamorphosis Figure 34.23 (a) Tadpole (b) During metamorphosis Figure 34.23 The “dual life” of a frog (Rana temporaria). (c) Mating adults 105

Figure 34.23a Figure 34.23 The “dual life” of a frog (Rana temporaria). (a) Tadpole 106

(b) During metamorphosis Figure 34.23b Figure 34.23 The “dual life” of a frog (Rana temporaria). (b) During metamorphosis 107

(c) Mating adults Figure 34.23c Figure 34.23 The “dual life” of a frog (Rana temporaria). (c) Mating adults 108

Fertilization is external in most species, and the eggs require a moist environment In some species, males or females care for the eggs on their back, in their mouth, or in their stomach © 2011 Pearson Education, Inc.

Figure 34.24 Figure 34.24 A mobile nursery. 110

Amphibian populations have been declining in recent decades The causes include a disease-causing chytrid fungus, habitat loss, climate change, and pollution © 2011 Pearson Education, Inc.

Concept 34.6: Amniotes are tetrapods that have a terrestrially adapted egg Amniotes are a group of tetrapods whose living members are the reptiles, including birds, and mammals © 2011 Pearson Education, Inc.

Ornithischian dinosaurs Dinosaurs Figure 34.25 Parareptiles Turtles Crocodilians Reptiles Archosaurs Pterosaurs Ornithischian dinosaurs Dinosaurs Saurischian dinosaurs other than birds Diapsids Saurischians Birds ANCESTRAL AMNIOTE Plesiosaurs Ichthyosaurs Figure 34.25 A phylogeny of amniotes. Tuataras Lepidosaurs Squamates Synapsids Mammals 113

Derived Characters of Amniotes Amniotes are named for the major derived character of the clade, the amniotic egg, which contains membranes that protect the embryo The extraembryonic membranes are the amnion, chorion, yolk sac, and allantois © 2011 Pearson Education, Inc.

Extraembryonic membranes Figure 34.26 Extraembryonic membranes Chorion Allantois Amnion Yolk sac Embryo Amniotic cavity with amniotic fluid Yolk (nutrients) Figure 34.26 The amniotic egg. Shell Albumen 115

The amniotic eggs of most reptiles and some mammals have a shell Amniotes have other terrestrial adaptations, such as relatively impermeable skin and the ability to use the rib cage to ventilate the lungs © 2011 Pearson Education, Inc.

Early Amniotes Living amphibians and amniotes split from a common ancestor about 350 million years ago Early amniotes were more tolerant of dry conditions than early tetrapods The earliest amniotes were small predators with sharp teeth and long jaws © 2011 Pearson Education, Inc.

Figure 34.27 Figure 34.27 Artist’s reconstruction of Hylonomus, an early amniote. 118

Reptiles The reptile clade includes the tuataras, lizards, snakes, turtles, crocodilians, birds, and the extinct dinosaurs Reptiles have scales that create a waterproof barrier Most reptiles lay shelled eggs on land © 2011 Pearson Education, Inc.

Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Figure 34.UN08 Cephalochordata Urochordata Myxini Petromyzontida Chondrichthyes Actinopterygii Actinistia Dipnoi Figure 34.UN08 In-text art, p. 715 Amphibia Reptilia Mammalia 120

Figure 34.28 Figure 34.28 Hatching reptiles. 121