History of Life 18 V. Vertebrates.

A. Archetypal Vertebrate.

1. Active swimmers; bilaterally symmetric. a. Segmented trunk muscles run the length of the ani- mal – contract one side at a time. Early Cambrian jawless fish, b. Notochord / vertebral col- Myllokunmingia recently dis- umn – support. covered in China. c. Muscles supported by ribs that attach to vertebral centra that surround the noto- chord. d. Hollow dorsal nerve (spinal) cord enclosed by vertebral arches extends backward to the tail from anterior brain – also hollow. e. Sense organs concentrated up front (cephalized): • Eyes: Two lateral (image forming) / One dorsal median (principally light-sensing). • Nose • Internal ears. f. No paired fins.

History of Life 19

2. Mouth leads to pharynx with gill slits. a. Internal gills used for filter feeding as well as respiration. b. Water flows in through the mouth, over the gills and then out through the gill slits. c. No jaws.

3. Primitive bladder / lung connected to pharynx – used for buoyancy / respiration.

4. Ventral heart pumps blood anterior to the gills where it is ox- ygenated and then delivered to tissues via arteries, arterioles, capillaries and then back to the heart. a. Second loop may have conducted deoxygenated blood to bladder / lung as needed, in which case, atrium may have been partially divided. b. In most modern fish, bladder / lung has become a swim bladder disconnected from pharynx. c. 2nd arterial loop – if it existed – lost.

5. Internal organs including segmented nephrons, in coelom – supported by mesenteries attached to ventral ribs – “tube within a tube” construction.

6. Post-anal tail extends beyond the coelom.

History of Life 20

Archetypal vertebrate in sagittal section. Note the dorsal nerve cord, notochord and pharyngeal gill slits. Vertebral column, ribs not shown. From Romer, A. S. 1964. The Vertebrate Body . W.B. Saunders. Phila- delphia.

History of Life 21 B. Invertebrate chordates. 1. Hemichordates – acorn (probos- cis) “worms” and pterobranchs. a. Three part body structure b. Proboscis captures food and di- rects to mouth, which is in the collar. c. Pharyngeal gill slits in trunk used for gas exchange. 2. Urochordates – tunicates (sea squirts) a. Motile larva; sessile adult. b. Extract food from water passing through gill basket using mu- cous secreted by endostyle 3. Cephalochordates – lancelets (Amphioxus ). a. Closest living form to a primi- tive chordate. • Segmented trunk musculature. Invertebrate Chordates. • Notochord. Top. Acorn worm (Hemi- • Gills / gill slits. chordata).. Middle. Tuni- • cate (Urochordata). A. Mo- Segmented gonads / nephridia tile larva with notochord. (excretory structures). B. Sessile adult with gill basket and endostyle. Bot- tom. Amphioxus . (Cepha- lochordata).

History of Life 22 b. More primitive than fish. Lacks • Brain / sense organs. • Respiration through skin. • Heart, capillaries, hemoglobin, RBCs • Sedentary. c. Filter feeder – endostyle secretes mucous as in tunicates. d. Fossils from Burgess Shale (mid-Cambrian).

B. One theory of chordate origins is that they arose from tunicate larva via neoteny. 1. Retention of larval notochord & trunk muscles. 2. Integration of gill basket / visceral structures with somatic structures (notochord / trunk muscles).

C. An alternative scenario is that tuni- cates are descended from a motile, Pterobranch. Note dorsal nerve cord and gill slit. bilaterian ancestor. In this case, 1. Sedentary habit of adults is a derived character 2. Larval motility reflects ancestral state.

History of Life 23

Tunicate larva scenario of vertebrate evolution.

History of Life 24 Early Vertebrate Evolution. A. Cephalochordate Origins.

B. Phylogeny according to Purves et al . Rejects 1. Freshwater origins. 2. Tetrapod descent from crossopte- rygians. Vertebrate phylogeny ac- C. Agnatha – Jawless fish. cording to Purves et al . 1. Date to Cambrian; common by Ordovician. 2. Had bony skeletons. 3. Lacked jaws / paired fins. 4. Ostracoderms. a. External head armor; possible defense against sea scorpions. b. In some, small spines at points where paired fins develop in more advanced forms. c. Cephalapsis type flattened dorso-ventrally with expanded Fossil Ostracoderms. From gill basket. Romer (1964). d. Hemicyclaspis had flipper-like structures in lieu of pectoral fins.

History of Life 25 5. Contemporary cyclostomes (lam- preys and hagfish) degenerate. a. Bony skeleton lost. b. Hagfish marine – bottom scaven- gers. • Lampreys anadromous. • Sessile, filter-feeding urochor- date-like larva. • Adults parasitize “real” fish. Devonian placoderms. A. D. Placoderms – first jawed fishes. “Spiny shark; B. Arthrodire. C. 1. 1st appear in Silurian; now extinct. Antiarch with pectoral flippers. 2. Jaws developed from gill arches. From Romer (1964).

3. Ossified skeleton / paired fins in some. 4. Several groups. a. Giant, giant parrot-beaked ar- throdires with jointed neck and head armor. b. So-called “spiny sharks” – acanthodians – close to ancestry Palaeoniscid chondrosteans. A. Extinct Palaeonsicus . B. of modern fish. Living Polypterus . From Romer (1964).

History of Life 26 E. Bony fish – two principle groups. 1. Actinopterygii – ray fins. 2. Sarcopterygii – lobe fins.

F. Actinopterygii. 1. Chondrosteii. a. Palaeoniscids. • Living example Polypterus – has paired, ventral lungs connected to throat, as opposed to a single, dorsal blad- der. • Suggests lungs a primitive bony fish trait. b. Paddlefish and sturgeons – mostly cartilaginous skeletons, feeble jaws – sensitive rostrum anterior to the mouth.

2. Holostei. a. Mid-Mesozoic origins. b. Spread from freshwater to ma- rine environments. c. Surviving forms are garpike and bowfin. 3. Teleosts. Chondrosteans. A. Paddlefish. B. a. Vast majority of living fishes. Sturgeon. From Romer (1964). b. Replace Holosteans by end of Mesozoic. c. Primitive forms include herring and salmonids. d. Advanced forms tuck pelvic fins under pectoral.

History of Life 27 G. Sarcopterygii.

1. Lungfish (Dipnoi)

2. Crossopterygii. a. Rhipidistians (Devonian). • Dominant FW predators. • Ancestral to tetrapods. • Fins evolved into limbs. b. Coaelacanths. • Secondarily marine. • Surviving Latimeria lives at Crossopterygians. A. Rhipidisian from the Devonian. B. Living Lat- depth. imeria . From Romer (1964).

History of Life 28

From fins to legs. Pectoral fin structure of recently dis- covered Tiktaalik is almost perfectly intermediate be- tween that of rhipidistian lobe fin fishes and the legs of labyrthinthodont amphibians. To the lobe fin humerus (red), radius (blue) and ulna (green), Tiktaalik adds dis- cernable wrist elements. From R. Dalton. 2006. The fish that crawled out of the water. Nature (published online 5 April, 2006 | doi 10: 1038/news060403-7).

History of Life 29 H. Labyrinthodont Amphibia. 1. Rhipidistian ancestry indicated by tooth structure unique to Rhipid- istians, Labyrinthodonts and Coty- losaurs (stem reptiles). 2. Shared characters: hinged brain- case; internal nares; pineal “eye.” Labyrthinthodont tooth 3. A good example of a case where in cross section. Note the grades are useful (IMHO). elaborate infolding of the dentine and enamel. I. Reptiles. 1. Dispensed with aquatic larval stage – amniotic egg . 2. Four principle groups distin- guished by temporal fossae. a. Anapsida – no opening – stem reptiles, turtles. b. Synapsida – lower opening – bounded above by postorbital and squamosal bones – mam- mal-like reptiles. c. Parapsida – upper opening – bounded below by postorbital Labyrinthodontia. A use- and s quamosal – extinct. ful paraphyletic group. d. Diapsida – two openings – rhyncocephalians (tuatara), Ar- chosauria (dinsoaurs, birds), lizards and snakes.

History of Life 30

Reptile Skull Types (schematic). A. Anapsid type – stem rep- tiles, turtles. B. Synapsid type – mammal-like reptiles. C. Par- apsid type– extinct pleisiosaurs, etc . D. Diapsid type – rhyn- cocephalians, dinosaurs, birds, snakes and lizards. From Romer (1964).

.

History of Life 31

Simplified schematic of the amniotic egg. Gas exchange with the ex- ternal environment via porous shell, which is impermeable to water, but not air.

History of Life 32 VII. Evolution of Mammals.

A. Synapsid reptiles antecedent to mammals. Include

1. Pelycosaurs (late Carboniferous, Permian). a. So-called “sail lizards” b. Dimetrodon , Edaphosaurus .

2. Therapsids (late Permian, early Triassic). a. Anomodonts – herbivorous forms. b. Theriodonts– “Mammal- like” reptiles i. Name - “beast-tooth” – reflects differentiation of teeth as observed in A therocephalian (cynodont sister mammals. clade) close to the ancestry of ii. Include cynodonts – di- mammals. rect ancestors of mammals.

Right. Overview of mammalian evolution. At present, it is generally believed that mammals constitute a monophyletic group, with therian (placental) mammals separating from non- therians (monotremes and marsupials) in the Jurassic. From Crompton, A. W. and F. A. Jenkins. 1973. Mammals from reptiles: a review of mammal origins. Ann. Rev. Earth Planet. Sci. 1: 131-155.

History of Life 33

History of Life 34 B. True mammals (and 1 st dinosaurs) appear in Triassic.

C. Theriodont evolution reflects acquisition of more active life style . 1. Locomotion . a. Legs tucked under the body. b. Chest deepened – anterior ribs expanded; posterior ribs lost. 2. Alternating contraction of trunk muscles replaced by “back and forth” motion of legs. 3. Tooth differentiation . a. Incisors, canines, premolars, molars; cusps on molars. b. Precise occlusion. 4. Bony secondary palette.

D. Hypertrophy of the coronoid process of dentary – tooth bear- ing bone of the lower jaw. 1. Correlated expansion of a. Temporal fossa. b. Jaw adductor muscles. 2. Reduction of post-dentary bones on the lower jaw 3. Replacement of articular-quadrate joint with dentary- squamosal.

History of Life 35

Hylonumus . Primitive anapsid from early Pennsylvaian Note sprawling gait. Length about 25 cm. From Ostrom, J. H. 1992. A history of vertebrate success. Pp. 119-139. In , Sachopf, J. W. Major Events in the History of Life . Bartlett Jones. Lon- don.

Thrinaxodon . An advanced early Triassic cynodont. Length about 60 cm. From Ostrom, J. H. 1992. A history of vertebrate success. Pp. 119-139. In , Schopf, J. W. Major Events in the History of Life . Bartlett Jones. London.

History of Life 36 Table 1. Some Reptile-Mammal Comparisons

# Character Reptile Mammal 1 Skull Fenestrae None Massive. 2 Braincase Loosely attached Firmly attached 3 Secondary pal- None Complete, bony ette 4 Dentition Undifferentiated Differentiated 5 Cheek teeth Uncrowned Crowned and points cusped 6 Tooth re- Continuous At most, once placement 7 Tooth roots Single Molars double- rooted 8 Jaw articula- Articular- Dentary-squamosal tion quadrate 9 Lower jaw Many bones Single bone 10 Middle ear Stapes Stapes, incus, mal- bones leus 11 External nares Joined Separate 12 Occipital con- Single Double dyle 13 Cervical ribs Long Reduced 14 Lumbar ribs Present Absent 15 Diaphragm Absent Present 16 Limbs Sprawled out Under body

History of Life 37 17 Scapula Simple Large spine for mus- cles 18 Pelvic bones Unfused Fused 19 Sacral verte- Two Three of more brae 20 Toe bone #s 2-3-4-5-4 2-3-3-3-3 21 Body tempera- Variable Constant ture

History of Life 38 E. Conversion of articular and quadrate bones to malleus and incus (middle ear bones) and angular to tympanic an- nulus . 1. One of the great examples of evolutionary transition.

2. In reptiles, the lower jaw consists of the tooth- Probainognathus . An advanced bearing dentary plus post- cynodont with a double jaw articu- dentary bones. lation. Modified from Carroll, R. L. 1988. Vertebrate Paleontology 3. Reptilian jaw hinge in- and Evolution . W. H. Freeman. volves articular (jaw) and NY. quadrate (skull).

4. With expansion of dentary, a. Post-dentary bones reduced. b. Dentary-squamosal hinge develops. c. Articular (malleus) and quadrate (incus) become middle ear bones.

5. Amazingly, intermediate forms with two functional joints have been found.

History of Life 39

Double jaw articulation in Probainognathus . The jaw joint is com- posed of quadrate and squamosal (upper) and articular and dentary (lower). Because the reptilian elements are still functional, this animal is considered to be a reptile. From Carroll (1988).

History of Life 40 F. All of these changes believed to have been driven by selection for 1. Higher activity levels , BMR, possibly reflecting greater reliance by mammals on aerobic respiration. 2. Enhanced high frequency hearing . 3. Questions remain as to degree of parallelism vs. synapomorphy in various therapsid lineages.

G. Therapsid extinction. 1. Therapsids were dominant tetrapods during the Permian. 2. Numbers decline during Triassic. 3. Two hypotheses : a. Outcompeted by dinosaurs. b. Opportunistic replacement mediated by extinction. 4. Fossil record does not permit us to distinguish between competive exclusion and environmentally-mediated extinction, but a. Considerable size overlap between therapsids and thecodont ancestors of dinosaurs. b. Virtually no overlap between mammals and dinosaurs. c. During the second half of the Trias, the lineages leading to mammals got small; while those leading to dinosaurs got large.

History of Life 41

Synapsid and Diapsid Reptiles in the Permian and Triassic. From M. J. Benton. 1983. Dinosaur success in the Triassic: A noncompetitive ecological model. Quart. Rev. Biol. 58 : 29-55.

History of Life 42 H. Mid-Mesozoic gap. 1. Mammalian grade of organization achieved by late Triassic. 2. For the most part, mammals remained small and insignificant for 150 million years. 3. Was what would otherwise have been a smooth progression from pelycosaurs to therapsids and cynodonts to placental mammals disrupted by the dinosaur interregnum?

I. Dino-enthusiasts point to the following postulated traits that could have resulted in archosaurian superiority: 1. Endothermy and high metabolic rate – at least in small predators. Deinonychus . A relative of 2. Sopohisticated social behavior: Velociraptor , star of Juras- a. Flocks / herds. sic Park . b. Pack hunting. c. Maternal care / family groups. d. Rapid locomotion. 3. Perhaps best explanation is that Mesozoic mammals remained small because larger ones would have been eaten.