Chapter 5: Evolution of Early Amniotes

When did amniotes arise + why?

due to climate shift from humid → dry near end of Carboniferous + Permian

Name two early amniotes

• Hylonomus and Paleothyris

• mid-Carboniferous of Nova Scotia

Early amniote cheek

• premaxilla and maxilla both have teeth

• squamosal, quadratojugal and quadrate make up posterior angles of the skull

Lower jaw/ mandible of early amniotes

• main lower jaw element in lateral view is the dentary at the front that bears the teeth

• behind it are the surangular above and the angular below

• jaw joint lies on the articular bone

The amniote skeleton

• lightly built skeleton

• the first two cervical vertebrae, the vertebrae of the neck, are highly modified to make the junction with the occipital condyle of the skull

• The cervicals bear short ribs → dorsal ribs longer→ rib cage

• astragalus

• hindlimbs + foot longer than forelimb and hand

• The pelvis → narrow ilium, and a heavy pubis and ischium ventrally, which meet each other in the midline as in early tetrapods

• no bony scales on skin → gastralia/ abdominal ribs closely spaced in belly region

Palaeobiology of the first Amniotes

• fed on invertebrates such as insects and millipedes→ teeth could pierce the tough cuticle to reach the flesh inside

• key feature of the skull of Paleothyris = increase in the strength of the jaws when compared with early tetrapods, sufficient to nip through the toughest arthropod cuticle

• in Paleothyris → heavy stapes as in the early tetrapods→ limited hearing → low‐frequency sounds

• It is unlikely that Paleothyris had a tympanum as there is no otic notch

• skeletons lightly built→ surprising that they were fossilised→ both found in fossilised tree trunks

• Hylonomus remains have been found in mudstones, sandstones, and coals, deposited in shallow freshwater lakes and rivers of the Cumberland Group of Joggins, Nova Scotia→ mid-Carboniferous → Joggins area covered with forests

When did amniote diversity/ numbers expand?

after Carboniferous Rainforest collapse 301-305 Ma + climate shift

Split in amniote evolution

• mid‐Carboniferous

• the Synapsida, leading eventually to mammals

• the Reptilia, including Parareptilia and Eureptilia (which includes Diapsida), which led to turtles, lizards, snakes, crocodilians and birds

Summary of Adaptations

1. control water loss (impermeable skin; salt concentration in excreted fluids)

2. walk on land (limbs offer support; complex nervous system)

3. feed on land (jaws adapted for holding and crushing food)

4. breathe exclusively in the air (efficient lungs; efficient circulatory system)

5. reproduce without the swimming larval stage or tadpole (amniotic egg; internal fertilization)

How is water loss in reptiles and other amniotes controlled?

• by managing water excretion through the kidneys and by having a largely waterproof skin

• amniotes conserve water through their specialized kidneys, where water is extracted back into the bloodstream, making the urine highly concentrated before it is shed

How can fish and amphibians in water release nitrogenous waste/ excess water?

dissolve nitrogen‐bearing residues from their food in copious amounts of water and then release the waste

How can reptiles and birds release nitrogenous waste/ excess water?

• concentrate their nitrogenous wastes and shed them as semi‐solid uric acid

• reptiles and seabirds also have salt glands located near the nose or eye through which they secrete a salty fluid as another means of regulating the concentration of their blood and bodily fluids, their osmotic balance.

Amphibian skin

• the skin of frogs and salamanders is soft and permits water to pass through, and they do not have scales → skin is often moist, and it oozes mucus to slow down water loss

• Some amphibians today also release peptides, poisonous substances, to protect themselves from skin parasites and disease‐bearing organisms →peptides are often brightly coloured to warn predators that they are poisonous, and indeed many frogs and salamanders in tropical areas feature bright colours in their skins also to warn predators to avoid them.

• Amphibian skin contains deposits of keratin → limits water loss and provides some mechanical protection from blows and rubbing.

• Amphibian keratin though is soft, unlike the hard keratin of amniotes.

Keratin in amniotes

• keratin is everywhere, forming layers within the skin, as well as tough, flexible structures such as the scales in reptiles, feathers in birds, and hair in mammals.

• Keratin also forms hard‐wearing, food‐chopping beaks in turtles and birds today, as well as in many extinct amniotes, such as beaks in Permian herbivores like the dicynodonts and many dinosaurian herbivores

Why do amniotes have a protective, waterproof integument?

• to limit water loss by evaporation through the body surface

• to protect against mechanical trauma

• to assist their locomotion.

Lizard skin

• double keratin layer, the thick horny epidermal scales on the outside, arranged in overlapping patterns, but linked underneath from scale to scale

• Below is the keratin‐rich stratum corneum, and then fibrous and loose connective tissue.

What does the dermal papillae in the skin regulate in different animals?

• reptiles: formation of scales

• birds: feathers

• mammals: hair

What kind of posture do most Mesozoic amniotes + birds and mammals have today?

parasagittal posture

Nervous + Sensory Systems of Amniotes

• amniotes → more complex nervous system

• crocodilians, birds, and mammals→ cerebral cortex

• higher‐order brain functions such as sensory perception, cognition, generation of motor commands, spatial reasoning, and languages

• most amniotes have good senses of smell and vision, and excellent hearing in some

What is the Jacobson’s organ?

• organ in roof of mouth of lizards + snakes

• detects smells by flickering tongue

Feeding in Amniotes

• at the origin of amniotes → feeding switched from suction to hunting prey with powerful jaws+sharp teeth or to herbivory

• underwater feeding → jaws just had to snap fast

• amniotes→ narrow snouts for fast but weak snapping, or broad snouts for slow but powerful chomping

• additional static force and manipulate the food using their jaws and tongues→ struggling prey or vegetation

Evolution of herbivory

• hard to evolve→ more costly → less nutrient rich → more energy spent on foraging etc.

• less dangerous than hunting (although plants can fight back e.g poison)

• vertebrates do not naturally possess the enzymes they need in their guts to digest plants, especially the cellulose in plants; these enzymes are found only in certain microbes and fungi

• baby herbivorous amniotes have to acquire these essential enzymes, either by eating worms or termites that already have the necessary enzymes in their guts, or even by eating their mother’s dung

Anatomical changes in amniotes due to dietary changes

• broadening of the skull at the back to allow for more powerful jaw muscles

• modifications of the teeth to become shorter and blunter, and sometimes arranged in multiple rows

• early herbivorous amniotes tended to become larger

How did devonian and carboniferous tetrapods breathe air?

buccal pump mechanisms

How do amniotes breathe?

• ribcage expansion

• no longer absorb oxygen due to waterproof skin

Circulatory systems in Amniotes

• amniotes→ higher blood pressure than amphibians

• birds + mammals → 2 separate/ double circulatory systems

• Crocodilians have partially divided ventricles, so the two blood flows are still kept apart, and even in lizards and snakes with a single ventricle, they have mechanisms to avoid too much mixing of oxygen‐rich and oxygen‐poor blood

• Efficiency → high blood pressure + separate blood flow

What is needed for reproduction on land?

• a way to fertilise eggs

• copulatory organ (penis0

• internal fertilisation as amniote egg enclose in a shell/ retained by female

Key features of the cleidoic egg

1. Semipermeable shell which allows gases to pass in (oxygen) or out (waste carbon dioxide) but keeps the fluids inside

2. Extraembryonic membranes:

   • The chorion (surrounds the embryo and yolk sac)

   • The amnion (surrounds the embryo with water)

   • The allantois (sac)

What do the chorion and amnion do?

function in protection + gas transfer

What does the allantois do?

• a sac involved in respiration + stores waste material

• as the embryo develops, the yolk sac, full of highly proteinaceous food, dwindles and the allantois fills up

Ancestral state of egg

• hard-shelled egg not ancestral state e.g snakes, many lizards, monotremes → mineralised slightly or not at all

• fossil hard‐shelled eggs are not known until the Late Triassic and Early Jurassic→ absence of evidence not evidence of absence but 100 Myr gap in amniote history

• phylogenetic study of egg evolution → first dinosaur eggs not mineralised → suggests soft-shelled eggs early origin

• viviparity is the dominant reproductive mode in mammals and in many marine reptiles, including possibly the Early Permian mesosaurs and that soft‐shelled eggs are laid by most lepidosaurs (lizards and snakes) as well as by early dinosaurs, suggests that the ancestral state was that Carboniferous amniotes either laid unmineralized eggs or retained their young for viviparous birth

viviparity

giving birth to live young

oviparity

production of eggs

Ovoviviparity

Ovoviviparous animals possess embryos that develop inside eggs that remain in the mother's body until they are ready to hatch

Extended Embryo Retention (EER)

• when the young are retained by the mother for a varying amount of time

• said to have adaptive advantages as developing embryo can be protected for a lesser or greater amount of time inside the mother, or birth can be delayed until environments become favourable

• Among modern lizards and snakes, closely related species can show different degrees of EER, and indeed in some cases, species seem to flip‐flop between oviparity and viviparity relatively easily

What could the mechanism of egg state evolution be connected to?

extended embryo retention

What are temporal fenestrae?

openings behind the orbit that are surrounded by the squamosal, parietal, postorbital, and jugal

Possible functions of temporal fenestrae

1. the provision of additional attachment edges for specific jaw muscles that allow jaw muscles inside the skull to bulge out

2. to reduce the weight of the skull and to conserve calcium

Anapsid skull

• no temporal fenestrae, a condition that is also plesiomorphic for tetrapods

• may include early forms such as Hylonomus and Paleothyris, as well as several lineages of parareptiles in the Permian and Triassic, and the turtles

• clade Anapsida not valid

Synapsid

amniotes with one lower temporal fenestra, surrounded by the postorbital, jugal, and squamosal

Diapsid

two temporal fenestrae, a lower one as in synapsids, and an upper one surrounded by the postorbital, squamosal, and parietal

Euryapsid

• present in a broad range of later amniotes, especially the marine nothosaurs, plesiosaurs, and ichthyosaurs of the Mesozoic.

• one upper temporal fenestra, surrounded by the postorbital, squamosal, and parietal

• pattern evolved from the diapsid by the loss of the lower temporal bar, as evidenced by the presence of a lower embayment in some early forms of these clades.

The Permian World

• supercontinent Pangaea

• Early Permian climates in the northern hemisphere were hot and arid

• Most finds of Late Carboniferous and Early Permian tetrapods are from the northern hemisphere, perhaps because the southern continents were experiencing cold and temperate climates.

• Across all tetrapods, the event marked the origins of major new dietary modes such as hypercarnivory (feeding on tetrapods) and herbivory, to add to the insectivory of earlier amniotes and microsaurs, and fish‐eating by larger tetrapods

• moist, vegetated areas between desert dunes

What are the 4 mass extinction events in the early evolution of amniotes?

1. Carboniferous Rainforest Collapse: 301-305 Ma

2. Olson’s extinction ~ 273 Ma

3. End‐Guadalupian mass extinction (or end‐Capitanian extinction), 259.1 Myr ago

4. Permian‐Triassic mass extinction

Carboniferous Rainforest Collapse

when wet‐loving early tetrapods such as the batrachomorphs and anthracosaurs declined in diversity and abundance, and the amniotes began to diversify, presumably having better adaptations to hot and dry conditions

Olson’s Extinction

which was marked by the global replacement of early synapsid faunas by therapsid‐dominated faunas

End‐Guadalupian mass extinction (or end‐Capitanian extinction)

• when the diverse and successful dinocephalians and the bradysaurine pareiasaurs died out

• Many other tetrapods died out, amounting to 74–80% loss of generic richness in the rich fossil beds of South Africa

• the crisis was followed by the diversification of dicynodonts, new clades of pareiasaurs, and gorgonopsians.

• extinctions among plants, as well as some species losses in the oceans.

• cause → eruption of the Emeishan volcanoes in South China, but the scale and importance of the event are debated

What two clades were reptilia split into?

Parareptilia and Eureptilia

What were the first fully aquatic amniotes?

Mesosaurs

Paleobiology of Mesosaurs

• long neck, body, flat-sided tail

• long thin jaws are lined with needle‐like teeth that intermesh as the jaws close → straining device that allowed Mesosaurus to take a mouthful of small arthropods or fish and strain the water out before swallowing

• fossil embryo reported → non-mineralised egg theory or viviparity as a means to protect young in early stages of development

• as a means of protecting the young in their early stages of development. There is evidence that the juvenile mesosaurs lived in shallow water, actively hunting their prey, and shifted to open water and began filter feeding as adults

What were the Eureptilia comprised of?

• early stem‐group clades and the Diapsida, represented today by lizards, snakes, crocodilians, and birds

• more long-lived than the extinct Parareptilia

What are synapsids the sister group to?

Reptilia (Parareptilia + Eureptilia)

When did synapsids originate?

Late Carboniferous

What 2 clades are synapsids generally divided into?

pelycosaurs and therapsids

Indications of herbivory from synapsids

1. teeth are spatulate in shape rather than pointed, and they have crinkled edges

2. the jaw joint is placed below the level of the tooth rows, an adaptation that shifts the maximum bite force to the cheek teeth

3. the jaw could probably have been moved fore‐and‐aft, and the barrel‐shaped ribcage presumably contained massive guts that were necessary for digesting large quantities of rough plant food

Pelycosaurs

groups of early permian sail-backed synapsids

Name a type of pelycosaur

Dimetrodon

Function of sails on pelycosaurs

• neural spines generally lie in a neat fence‐like array, which suggests that they were held together by a tough covering of skin in life.

• the ‘sail’ then was probably composed of heavily vascularized skin, and its function has often been interpreted as thermoregulatory

• most pelycosaurs lacked sails and survived fine though

• sail presence does not correlate with body size, and the bone histology does not support a thermoregulatory function, so they might have been species recognition adaptations, like particular colours or crests in mammals and birds today

What are therapsids?

clade diagnosed by an enlarged temporal fenestra, loss of the supratemporal bone, a deeply notched reflected lamina on the angular bone, an anterior position of the jaw joint, reduction of the palatal teeth, as well as modifications of the shoulder and pelvic girdles and of the hindlimb

Example of an early therapsid

Dinocephalian

What other therapsids replaced Dinocephalia in the Middle Permian?

gorgonopsians and dicynodonts

Dicynodonts

• dominant herbivores in Late Permian

• some were burrowers, others diggers

• nearly all died in Late Permian→ passed through bottleneck and radiated in Triassic

Gorgonopsids

• dominant carnivores of Late Permian

• vast canines, jaw could open 90 degrees

Therocephalia

• carnivorous therapsids

• Middle Permian → middle Triassic

• Survived P-Tr ME

• ranged in size from small insectivores to large carnivores, and also include some herbivores in the Early Triassic

Cynodonts

• includes mammals

• arose end Permian + radiated in Triassic

• example = Procynosuchus

When was the P-Tr ME?

251.9 Ma

How long did the P-Tr ME last?

60,000 years

Cause of P-Tr ME

Volcanic eruptions in Siberia → Siberian Traps → represent massive volumes of basalt lava erupting in several bursts through a span of 0.9 Myr

Consequences of Siberian Traps on land

• acid rain was a consequence of the huge influx of gases into the atmosphere, and this killed trees, and plants in general

• Without their stabilizing root systems, soil was massively removed from the land and washed into the sea, and this is indicated by major changes in fluvial systems in terrestrial rock sequences across the PTB, from gentle, meandering streams in the latest Permian to rapid‐flowing braided streams and alluvial fans in the earliest Triassic

• coal gap for the first 10 myr of Triassic

hyperthermal event

when high levels of greenhouse gases in the atmosphere led to sharp global warming, acid rain, ocean acidification, and seabed anoxia, which in turn caused extinction of life.

Temperature rise during PTr

• temperature rise of 10–15 C

• this raised equatorial air and ocean temperatures from 25 C to 35–40 C

Consequences of the PTr in the Oceans

• masses of sand and mud doubtless killed shallow‐water filter feeders.

• the heating of the surface waters probably slowed down ocean circulation in which cold polar waters skim along the seabed and rise at the equator, where they pick up oxygen, and bring it back down to the seabed.

• worldwide anoxic episode at the beginning of the Triassic, where sediments are all black, full of carbon, and often associated with sulphur minerals such as iron pyrites → indicates absence of oxygen

• earliest Triassic marine sediments are often virtually empty of life: in the many sections that span the PTB, life appears to have been rich and diverse immediately before the event, and then the burrowers, the seabed dwellers, the reef‐builders, and the animals that swam above the sea floor are all gone

Early Triassic Ecosystems

• Late Permian dominated by herbivorous pareiasaurs and dicynodonts and carnivorous gorgonopsians → replaced by new clades of archosaurs (crurotarsans, dinosauromorphs) and synapsids (cynodonts)

• extinction rates remained high over an interval of up to 1 Myr, beginning sometime before the PTB, and continuing high into the earliest Triassic

• At this point, origination rates of tetrapods also increased, corresponding to a time of rapid turnover immediately after the peak of extinction

• Many disaster taxa e,g dicynodont Lystrosaurus