Tetrapods: The First Steps Along Our Path

What Makes a Vertebrate?

  • Recommended reading: Benton & Harper 2020: Ch. 17, 18 2009: Ch. 16, 17.
  • Chris Mays provided assistance.

Lecture Summary

  • What makes a vertebrate?
  • Early chordates
  • The age of the fishes
  • The first steps on land
  • Challenges & solutions
  • Why (AKA: what adaptive advantages)?
  • Tetrapods
  • (Proto-)mammals
  • In the shadows of dinosaurs
  • The age of mammals

Chordates

  • Something that we share.
  • Chordates: notochord, neural chord, postanal tail.
  • Reference: Martinez-Morales (2015). Brief. Funct. Genom. 2015: 1–7.
  • Body plan: a lancelet (a non-vertebrate chordate).
  • Looks like Pikaia! (Cambrian, 500 Ma).

Vertebrates

  • Vertebrates – subgroup of Chordata: All chordate bits + (reinforced) branchial/gill arches, neural crest, brain!
  • Apatite (Ca-phosphate, e.g., bone, teeth), cartilage (e.g., sharks).
  • Body plan: a lamprey (a vertebrate chordate).

Earliest Chordates

  • References: Conway-Morris & Caron (2012). Biol. Rev. 87: 480–512; Tian et al. (2022). Science 377: 218–222.
  • Earliest chordates: ?Pikaia… (~505 Ma, mid-Cambrian), Canada.
  • Pikaia gracilens: 520–505 Ma.

Cambrian Burgess Shale

  • Amidst the Cambrian carnage: an ancestral form of Phylum Chordata.
  • Highlights the contingency of evolution.
  • Pikaia gracilens: The ancestral group of this is represented by this.

Lagerstätten

  • Earliest chordates: ?Pikaia… (~505 Ma, mid-Cambrian), Canada.
  • Or Cathaymyrus (518 Ma, e Cambrian), China.
  • Earliest vertebrates: Yunnanozoans (518 Ma, e Cambrian), China.
  • References: Conway-Morris & Caron (2012). Biol. Rev. 87: 480–512; Tian et al. (2022). Science 377: 218–222; Sansom et al. (2010). Nature 463: 797–800.
  • “Lagerstätten”: Rare soft-tissue windows into our squishy past.
  • Incredibly unlikely preservation… Huge gaps in evo story between them! But… chordates SHOULD come first!

Evolutionary Timeline

  • Evolutionary timeline: Collagen à cartilage à bones/teeth
  • Agnathans (=jawless): oldest fish
  • Cartilaginous: Early Cambrian (518 Ma)
  • Teeth elements (conodonts) by mid-Cambrian (510 Ma)
  • Age of Fishes.
  • References: Murdock et al. (2013). Nature 502: 546–549; Terrill et al. (2018). J. Analyt. A. Spectro. 33: 10.1039/c7ja00386b.
  • Benefits of mineralised hard parts?
  • Early functions of apatite à ‘appetite’!
    • Teeth
    • Muscle attachment (incl. jaws)
    • Armour

Gnathostomes

  • Gnathostomes (=jawed mouths)
  • Jaws à from branchial arches (hardened by cartilage/bone)
  • Classic case of ‘exaptation’: à shifted trait function
  • Theory based primarily on homology of modern fish
  • Earliest ‘proto-jaws’ probably not mineralised àNo clear fossils of this
  • MC tells us first jaws: à Ordovician (~480 Ma)
  • Reference: Simakov et al. (2020). Nature Eco. Evo 4: 820–830.

Oldest Jawed Fish

  • Oldest jawed fish: Placoderms
  • Oldest fossil à Silurian (435 Ma)
  • ‘Teeth’ are modified sharp bony plates
  • Peak predators of the Devonian seas
  • Armoured bony plates à vertebrate arms race?
  • ±Extinct: end-Devonian mass extinction event
  • References: Zhu et al. (2022). Nature 609: 954–958; Sallan et al. (2010). PNAS 107: 10131–10135.
  • Dunkleosteus size comparison.

Extant Fish Groups

  • Two main extant fish groups:
    • Cartilaginous fish (chondrichthyans): e.g., sharks, rays; First emerged in Ordovician/Silurian (~440 Ma)
    • Bony fish
      • Ray-finned fish (actinopterygians): most abundant + diverse modern group
      • Lobe-finned fish (sarcopterygians): Sister group to tetrapods (like us!) + lungfish; Bony fish groups split in the Silurian (~425 Ma)
  • All of the above:
    • Filled placoderm niches after end-Dev extinction à Ecological vacancy
    • MAJOR diversification (Carboniferous ~300 Ma)
  • The very finny “Lazarus taxon” Devonian–Cretaceous… & today Coelacanth (Latimeria).
  • References: Coates et al. (2018). Proc. Roy. Soc. B 285: 20172418; Lu et al. (2017). Nat. Comms 8: 1932.

Fish Examples

  • Ray-finned fish: Cheirolepis (M Devonian; ~395 Ma).
  • Lobe-finned fish: Gaiyu (Late Silurian; ~425 Ma); Diabolepis (E Devonian; ~415 Ma).
  • Cartilaginous fish: Tezakia – fossil bony denticles (L Ordovician ~490 Ma).
  • References: Andreev et al. (2015). Palaeontology 58: 691–704; Mondéjar-Fernández et al. (2020). J. Vert. Paleo. 40: e1772274; Lu et al. (2016). Current Biology 26: 1602–1608; Zhu et al. (2009). Nature 458: 469–474.

First Steps

  • Oldest tetrapod fossils: trackways! (?420–)385 Ma.
    • Zachelmie, Poland, Mid-Devonian (~393 Ma)
    • Valentia Island, Co. Kerry, Mid-Devonian (~385 Ma)
    • ‘Glenisla’ Homestead courtyard, Australia L Silurian–E Devonian (~420 Ma!!)
  • Problems:
    • Provenance
    • Age (too old!)
    • Trackmaker ID (?)
  • References: Stössel (1995). J. Geol. Soc., London 152: 407–413; Niedźwiedzki et al. (2010). Nature 463: 43–48; Warren et al. (1986). Alcheringa 10: 183–186; Young (2006). Alcheringa Spec. Iss. 1: 409-428.
  • “Tetrapod” = four legs à first land-walking vertebrates.

Challenges of Moving to Land

  • The challenges (Vertebrates 385–360 Ma):
    • Locomotion à Very different motions required (stepping vs swimming)
    • Sensory perception à In air: sound travels poorly, need to see further (+low P)
    • Support against gravity à Water = 1000x denser than air: 1000x times ‘heavier’ in air!
    • Tissue & offspring desiccation à Solution: water-retentive skin and, much later, eggs (e.g., amniotes)
    • UV damage à Solution: Increase in skin melanin (UV photoprotection)
    • Water and nutrient uptake and distribution à Vertebrates are mobile & have vascular system
    • Gas exchange à Early bony fish had lungs AND gills
  • References: Ahlberg (2018). Earth & Enviro. Sci. Trans. Roy. Soc. Edinburgh 109: 115–137; McNamara et al. (2019). Trends Ecol. & Evo. 36: 430–443.

Support Solutions

  • Vertebrate bodies are mostly H20 à buoyant under water. In air: Gravity sucks…
    • Structural support for organs
    • Need support off the ground
  • Solutions:
    • Reinforced ribcage
    • Enlarged & heavily modified limb bones & musculature
  • Challenge A: Support (385–360 Ma).
  • Reference: Molnar et al. (2018). Biol. Revs 93: 1077–1107.
  • Homology diagram: Lobe-finned fish -> Stem tetrapod (Acanthostega) -> Modern amphibian (salamander).

Locomotion Solutions

  • VERY different movement requirements on land (Vertebrates 385–360 Ma):
    • Water: mainly forward propulsion needed à primarily tail
    • Land: support and propulsion à primarily (hind)limbs
  • The “wheelbarrow model”.
  • Solutions:
    • (+ support muscles + bone restructuring)
    • Pectoral + pelvic fin modification
    • Elongated proximal limb bones
  • Fossil evidence: clear homology pathway between lobe-fin fish and tetrapods
  • NOT a feasible step for ray-fin fish…
  • Challenge B: Locomotion.
  • Homology diagram Ray-finned fish Lobe-finned fish
    Swimming Walking
  • References: Pierce et al. (2013). Integrat. & Compar. Biol. 53: 1–15; Woltering et al. (2020). Sci. Advances 6: eabc3510; Molnar et al. (2018). Biol. Revs 93: 1077–1107.

Sensory Perception Solutions

  • Sound in air à slower & shorter range… Longer vision needed for predators/prey (Vertebrates 385–360 Ma).
  • Solutions:
    • Hearing: Hyomandibula (jaw bone) à stapes
    • ANOTHER exaptation of gill arches!
    • Tympanic ear (ear drum): evolved ≥4 separate times
    • Sight: Increase in eye size, migrate to top of head
    • ‘Buena vista’ hypothesis: preceded full land-dwelling, helps hunting from water, no downside in water
  • Challenge C: Sensory perception.
  • References: Clack et al. (2003). Nature 425: 65–69; Brazeau & Ahlberg (2006). Nature 439: 318–312; Clack (2002). J. Neurobiol. 53: 251–264; MacIver et al. (2017). PNAS 114: E2375–E2384.
  • Tiktaalik vision.

Colonization of Land

  • By mid-Devonian, our ancestors were ready to colonise this unexplored new world…What did we see?
  • (Vertebrates 385–360 Ma)
  • What took us so long?
    • Rhyniognatha (~410 Ma; 25 Myrs earlier!)
    • Land plant spores (~450 Ma; 65 Myrs earlier!!)
  • Reference: Ahlberg (2018). Earth & Enviro. Sci. Trans. Roy. Soc. Edinburgh 109: 115–137.

Why Move to Land?

  • So many challenges: Why? Or why then? (Vertebrates 385–360 Ma)
    • Lands vegetated and inhabited by arthropods for >25–65 Myrs à Plenty of food sources
    • Escaping intermittent drought à The ‘freshwater first’ hypothesis
    • Devonian decreasing O2 trend à Easier to absorb oxygen from air than water
    • Escape! à No other vertebrates: no direct competition, no predators
    • Others…? Warning: conjecture zone!

Tetrapods Take Over

  • Tetrapods took over the continents.
  • With a bit of Carboniferous competition…Amphibians.
  • Amniotes (AKA: snacks).
  • Tetrapods (crown groups).

Amniotes Differentiation

  • Amniotes (terrestrially-adapted egg, claws, land-only life cycle).
  • Differentiating amniotes: it’s all in the head.
  • Lissamphibians.
  • Synapsids.
  • Diapsids.
  • Pelycosauria.
  • Therapsids.
  • Cynodontia.
  • Sauropsids.

Synapsid Diversity Through Time

  • Paleozoic.
  • Mesozoic.
  • Cenozoic.
  • Amphibians.
  • Turtles.
  • Birds.
  • Reptiles.
  • Mammals.
  • Advanced mammals.
  • Diapsids.
  • Primi mami.
  • Therapsids.
  • Pelycosaurs.

Synapsid History

  • Early Permian.
  • Middle Permian.
  • Late Permian.
  • Early Triassic.
  • Middle Triassic.
  • Late Triassic.
  • Earliest pelycosaur fossils from ~315 Ma.
  • Reference: Kardong 1998.
  • Dimetrodon.

Pelycosaur Skulls

  • Pelycosaur skulls display key synapsid features shared with mammals (including us!).
  • Differentiating synapsids: with differentiated teeth.

Therapsida

  • First therapsids from ~270 Ma.
  • Include carnivores and the first vertebrate herbivores.
  • Dominated mid-late Permian terrestrial ecosystems.
  • Includes mammals!
  • Synapsid history.
  • Reference: Kardong 1998.

Cynodontia

  • First cynodonts from ~255 Ma.
  • Early cynodonts have had many mammal-like features, incl. evidence of facial whiskers hence fur à endothermy?!
  • Reference: Benoit et al. (2020). J. Mammal. Evo. 27: 329–348.
    *Just in time for the worst event in history…

End-Permian Event

  • The end-Permian event (252 Ma).
  • Vertebrate tracks & burrows.
  • Burrows: ‘Aestivation’.
  • We are descended from cowards!
  • Reference: McLoughlin, Mays et al. (2020), Palaios 35: 342–357.
  • Survivors of the ‘dead zone’.

First Mammals

  • First mammals ~ Late Triassic (225 Ma).
  • References: Benoit et al. (2020). J. Mammal. Evo. 27: 329–348; Cabreira et al. (2022). J. Anatomy 241: 1424–1440.

What Is a Mammal?

  • Mammals.
    • Hair
    • Milk
    • Single lower jaw bone
    • Simplified jaw joint
    • Three middle ear bones à New function of old jaw bones à A 3rd exaptation of our old gill arches… our inner fish again!
    • Greater teeth differentiation
  • What is a mammal?
  • Far more likely to preserve in fossils!

Mammals in the Mesozoic

  • Mesozoic: >70% of mammal history (~160 Myrs).
  • Mammals & dinosaurs originated in Triassic
  • Mammals diversified throughout
  • But most Mesozoic mammals
  • Reference: Close et al. (2025), Current Biology 25: 2137–2142.
  • In the shadows of dinosaurs.
  • So, why did dinosaurs dominate the Mesozoic?

Competition Between Mammals and Dinosaurs

Repanomamus turns the table.

Mammal Domination Mystery

  • Mesozoic: >70% of mammal history (~160 Myrs).
  • Mammals & dinosaurs originated in Triassic.
  • Mammals diversified throughout.
  • But most Mesozoic mammals
  • Ecological exclusion (competition)?
  • Probably, but: why were mammals excluded?
  • Physiological exclusion?
  • Over-heating (no body cooling adaptations)
  • But evidence of burrowing & endothermy…
  • Unable to digest Mesozoic foliage?
  • NOT a problem at all…
  • So, why did dinosaurs dominate the Mesozoic?
  • Reference: Close et al. (2015). Current Biology 25: 2137–2142; Kemp (2017, ed.). Mammals: A Very Short Introduction: Oxford University Press.
    *Still a major mystery…

Teeth

  • Enamel is hardest substance in mammal body
    • Mohs hardness = 5 (b/w steel & titanium) à outstanding preservation potential
  • Complex:
    • Rich in morphological features to trace lineage
  • Shape of teeth varies with mechanical properties of food à fossil shape tell us about diet

Tooth Complexity

  • Foods vary in difficulty of mechanical breakdown
    • Prediction: ↑ in processing capability to compensate
    • ↑ processing capability by ↑ number of features on tooth
    • Roughness or ‘complexity’ of tooth surface

Similarities in Tooth Trends

  • Extensive differences:
    • Ecological niches
    • Physiology
    • Body sizes
    • Evolutionary histories
    • Details of cheek tooth shape
    • Numbers of teeth
    • Tooth classes
    • Chewing motion
  • Despite these, similarities in tooth trends (observable in fossils):
    • Broad range of dietary habits that evolved repeatedly
    • i.e., carnivory à herbivory

Adaptive Radiation

  • Early Cenozoic (66–55 Ma)
  • Explosion in mammals:
    • Diversity
    • Ecological niches
    • Abundance
    • Geographic distribution
    • Individual sizes
    • Specific mechanisms…? à still debatable
  • The age of mammals
  • (One of the cleanest examples of adaptive radiation)
  • You are here. More with Tom Reed.
  • References: Benton (2014). Vertebrate Palaeontology, 4th Edition. Wiley-Blackwell, 480 pp; Kemp (2017, ed.). Mammals: A Very Short Introduction: Oxford University Press.

Adaptable Ancestors

  • Our ancestors:
    • Surviving, if not thriving!
    • Humble
    • Relatable
    • ‘Lucky’
    • Carboniferous amniotes
    • Devonian tetrapods
    • Cambrian chordates
    • Mesozoic mammals
  • Our path: conclusions
  • Our ancestors Adaptable!

Ocean Innovations

  • Ocean innovations
    • Neural chords/brain
    • Reinforced branchial arches à jaws - Exaptation
    • Biomineralised internal skeleton
    • Equipped for land
      • Reinforced ribcage
      • Enlarged & modified limbs (incl. wrists/ankles)
      • Enlarged eyes
      • Hyomandibula à stapes - Exaptation
    • Road to Mammalia
      • Simplified jaw à all inner ear bones - Exaptation
      • Adaptable teeth
        Age of the mammals… had to wait!