Origin of Tetrapoda

John Merck

Link to cladogram and phylogram cheat-sheets

Elpistostegalia becomes "digitized"

We have discussed the elpistostegalians Panderichthyes and Tiktaalik from the late Frasnian stage of the Devonian, a time of low oxygen concentration. They next appear in the earliest Fammenian stage with Parmastega aelidae, known from skull and pectoral girdle elements (Beznosov et al., 2019.)

Parmastega aelidae from Beznosov et al., 2019. Scale = 1 cm.

Parmastega has enlarged, dorsally placed orbits, and seems to have hunted with its eyes and skull table protruding from the water. It's nostrils faced downward, but like other elpistostegalians, it could have breathed through its spiracles. It's forelimbs aren't preserved, but its pectoral girdle resembles those of later elpistostegalians with digits. Known only from its skull and girdle elements, Parmastega lacks opercular elements and the dermal pectoral elements dorsal to the anocleithrum. Thus, like Tiktaalik, it had a neck of sorts. Potential synapomorphy with Tetrapoda:

When we meet elpistostegalians again in the latest Devonian, O2 concentrations had returned to familiar levels, but air-breathing adaptations had not gone away. Progressing into the Carboniferous - the "Age of Oxygen," the atmosphere became the place for easy access to O2, creating a selective pressure to exploit air-breathing abilities.

We now encounter creatures with very tetrapod-like heads including Ventastega curoni (Ahlberg et al., 2007).

What kind of appendages attached to the pectoral girdle? Unknown. Fortunately in the next case, it is not.

Acanthostega gunnari from Clack 2012
Acanthostega gunnari (Latest Devonian):

Very well known from relatively complete skeletons. The first and phylogenetically most basal vertebrate definitely to possess fingers and toes! Synapomorphies with Tetrapoda include:

Neurocranium of Acanthostega gunnari from Clack 2012
Acanthostega's neurocranium at last begins to resemble that of a tetrapod. Note:

Acanthostega gunnari skull from tumblr
But was it a fish? Consider the transformations listed at the beginning of the lecture:

The overall impression is of a fully aquatic animal with rudimentary ability to support some body weight on fore and hindlimbs and with the beginnings of the ability to use its jaw and hyoid arch to pick up sound from the ground. Maybe it came onto land occasionally to feed, disperse to new habitats, or thermoregulate, but it was primarily an aquatic animal. What did it use its fingers and toes for? Maybe not much at all. As with the origin of lungs in Osteichthyes, Byrne et al., 2020 speculate that the evolution of digits might be a response to high tide ranges and the hazards of becoming trapped in tide pools.

Ichthyostega stensioi
Ichthyostega (Latest Devonian):

Very well known (even in popular culture of previous generations: See Album cover of Yes' "Tales of Topographic Oceans" by Roger Dean) from relatively complete skeletons, but redescribed by Ahlberg et al., 2005.

Ichthyostega is the first animal we have seen with unambiguous adaptations to leaving the water: It's limbs, however, although more powerful than those of Acanthostega were paddle-shaped and probably did not offer much help out of the water. Maybe it lurked near the water's edge and lunged at prey on shore, or hauled itself up onto the beach in the manner of a harbor seal (Link to video). In short, it probably came onto land briefly but neither it nor Acanthostega could really walk on it.

Tulerpeton curtum scale bar = 1 cm.
Tulerpeton curtum: (Latest Devonian) Significant but known only from pectoral and fore and hindlimb elements, along with belly scales. Derived features include: Tulerpeton's limbs appear to be adapted to use as paddles for swimming, but it seems to have been an air-breathing adult with an increased ability to halt the production of fingers at an early stage.

Elegant Hypothesis - Brutish Facts: We have constructed an attractive and coherent picture of the steps in the acquisition of tetrapod-like attributes:

But there are at least two problems:

Chastened, we consider the Carboniferous: Remember, the latest Devonian "digitized" elpistostegalians weren't, as far as we can tell, really using their digits for much. From these beginnings, creatures had three general options:

Each strategy is reflected in Carboniferous elpistostegalian diversity.

Oestocephalus amphiuminus

(Early Carboniferous - Early Permian) Superficially snake like, elongate, and limbless (Although Phlegethonia retains a cleithrum in the pectoral region (Anderson, 2002). Long regarded as members of crown Tetrapod, Pardo et al., 2017 found to be early stem tetrapods (ironically) based on ancestral features including:

Their removal to the stem of Tetrapod is much more stratigraphically congruent than their previous placement.

Oestocephalus amphiuminus from Carroll 2009
Skulls are significantly modified, with orbits shifted far anteriorly and jaw articulation shifted posteriorly resulting in the great elongation of the temporal region. What's particularly strange is the reduction and fragmentation of the dermal bones of the temporal region. To compensate for the loss of mechanical strength that this implies, the palatoquadrate actually ossifies as a single unit.

Aistopod vertebrae are holocentrous, however Lethiscus, from the Early Carboniferous, was found by Anderson et al., 2003 to retain distinct intercentra and pleurocentra. It seems to be the most primitive aistopod. Alas, being so highly derived, the paleobiology of aistopods is difficult to interpret. Because descriptions of branchial arches and pectoral girdle (such as it is) are lacking, we can't even assess whether they were primarily air breathing.

Pederpes finneyae from Palaeos.
Whatcheeridae: Clack, 2002 described Pederpes finneyae of Britain, from the middle of Romer's Gap at 350 mya. Although it retains a tiny sixth finger, has a robust lateral line system, a heavy hyomandibula/stapes, and retains a preopercular; it also has robust limbs and a skull that is compressed from side-to-side like early land vertebrates. It and close relative Whatcheeria comprise the Whatcheeriidae (Latest Devonian - Early Carboniferous). We don't know how much time they spent on land, but it seems, at least, to have been able to walk - a new development fifteen million years after the evolution of hands and feet. Otoo et al., 2021 note that in comparison to other basal tetrapods, whatcheeriids have extremely large robust limbs, but that they present plausible adaptations to aquatic life.
Early Carboniferous Landmarks: Emerging from Romer's Gap, we pick up several lineages. Their synapomorphies:

Greererpeton burkemorani from Carroll, 2009.
Colosteidae: (Carboniferous) Including the familiar Greererpeton. All are elongate with small limbs whose joints are formed in cartilage. They retain extensive lateral line systems, and some have gill-rakers on their ceratobranchials, indicating an open operculum and suspension feeding as an option (Schoch and Witzmann, 2011). Distinctly fresh-water aquatic. Distinctive features:

Crassygyrinus scoticus from Theclacks.org. Total length~35 cm..
Crassygyrinus scoticus: (Early Carboniferous) Very strange: Indicates a permanently aquatic animal. The skull combines derived and primitive features: Placed in a compromise position on our cladogram, but different analyses differ wildly about where it should go.

Loxomma allmani from Palaeos. Total length~25 cm..
Baphetidae:(Carboniferous) A morphologically disparate but distinct clade of aquatic predators. Known since the 19th century from skulls but hardly any postcranial material. Plesiomorphic in retention of full lateral line system and distinct spiracular notch.


What was housed in this embayment is a topic of wild speculation:

Baphetid diversity: encompasses several ecomorphs.

Phylogenetic analyses place baphetids either below the base of crown Tetrapoda or as basal members of the Lissamphibian stem. A potential synapomorphy of baphetids and the lissamphibian line: A slender hyomandibula suspended in the spiracular chamber - except now we can start saying "A slender stapes suspend in the middle ear."

Eoherpeton watsoni an Early Carboniferous anthracosaur from Carroll 2009.
Anthracosauria: (Carboniferous - Triassic) Aquatic to mostly terrestrial vertebrates of the late Paleozoic. Although this groups membership varies with each new publication, it seems monophyletic.

Identifying characters:

Relationships: Until recently seen as the basal members of Reptiliomorpha. Some characteristics, including the tabular parietal contact and the large pleurocentra are shared with other reptiliomorphs, including amniotes. However recent analyses have placed them outside of Tetrapoda, in part due to the persistence of plesiomorphies like caudal fin rays (Clack, 2011).

Embolomere localities track Late Paleozoic "Coal Swamp" rainforests from Chen and Liu, 2020.
Anthracosaur superlative: Embolomeri: (Carboniferous - Late Permian) A speciose group including aquatic predators characterized by fully embolomerous vertebrae - intercentra and pleurocentra disk-shaped and roughly equal. These included eel-shaped aquatic predators of the Carboniferous and Permian such as Archeria (from Holmes, 1989) and Pholiderpeton. As Chen and Liu, 2020 note, the range of fossil occurrences of embolomeres tracks the distribution of "coal swamp" style equatorial rainforests.

Final word:

Stem tetrapods are paradoxical. All show adaptations indicating increased reliance on air-breathing, the hearing of airborne sound, and some may have routinely walked on land; however Acanthostega, Greererpeton, Whatcheeria, and Megalophalus, all display osteological correlates to the presence of internal gills (Schoch and Witzmann, 2011). Thus, no matter how much time they spent out of the water, they remained fundamentally aquatic.

The Devonian extinction seems to have wiped out the water-breathing digit-bearing vertebrates like Acanthostega and Ichthyostega, however many basal stegocephalians held on in the Early Carboniferous. Among them was the (unknown) last common ancestor of all living land vertebrates - the ancestor of crown-group Tetrapoda. Their common ancestry is concealed within Romer's Gap. Their descendants (along with some "stem tetrapod" lineages emerge from it well-differentiated.)

Tetrapoda: Opinions vary as to where this name should be stuck to the tree:

For our purposes, the crown-group definition applies.


Phylogeny: Tetrapoda consists of two major lineages with living members:

Greererpeton burkemorani
Noteworthy plesiomorphies - Evolving sensory modalities: Mentioned previously, all of the special senses needed to be adjusted for life on land. For most, these changes left no fossil record (vision, olfaction). In two, however, there are clear osteological correlates. :

Additional reading: