Stegocephali: Adaptations to land


Context:

Today we examine the transition to life on land, which was achieved by members of Sarcopterygii, the lobe-finned fish.


Eusthenopteron foordi Raul Martin
Tristichopteridae: Our starting point is the well-understood fossil tristichopterid Eusthenopteron foordi (Late Devonian) A group of choanate fish (i.e. with external nares and internal choanae) ranging from the Devonian to the early Permian. they are interesting to us as indicators of what the last fully aquatic ancestors of land vertebrates might have looked like. Fortunately, the anatomy of some, such as Eusthenopteron, is very well know from many excellent fossils.



Panderichthys rhombolepis B. D. Bogdanov from Wikipedia
Panderichthys: This is an example of a small group of fish-like vertebrates even closer to the common ancestry of land vertebrates than tristichopterids:

Definitions:

Somewhere between Panderichthys and the last common ancestor of Tetrapoda, vertebrates emerged onto land. They didn't have to. This required a bigger set of adaptations than the acquisition of warm-bloodedness in synapsids. What obstacles did they overcome to do so?


From Palaeos
The biological significance of the invasion of land.

Roster of transformations.


From Hybrid birder
  • Reproduction and life history:


    Landmarks in evolution of terrestriality


    Eusthenopteron foordi from Palaeos
    Our starting point: Eusthenopteron foordi (Late Devonian), a purely aquatic freshwater predator with no adaptations to life on land.



    Tiktaalik roseae from Villanova University
    Tiktaalik roseae: (Late Devonian) First published in 2006, this creature has become the new poster-child of vertebrate evolution. It is featured in:

    In its general profile, it's similar to Panderichthys, but there are two important differences.

    A description of Tiktaalik's pelvis was published in 2014. Although the hindlimb is unknown, the pelvis is surprisingly large and the hip socket is circular, indicating that the hindlimb was strong and had a wide range of motion. And yet, Tiktaalik lacked a sacrum.

    From this it seems that Tiktaalik could support at least a little of its weight on its paired fins. What would be the point? For an idea, we look at the head.


    Tiktaalik roseae from Clack, 2012
  • The neck: Tiktaalik lacks:

    As a result, its skull and pectoral girdle were no longer in contact, allowing the head to be flexed with respect to the torso - the beginnings of the neck.



    Spiracles of a tristichopterid and a basal elpistostegalian compared from Brazeau and Ahlberg, 2006.
    Spiracular inspiration? The earliest elpistostegalians (including Panderichthys and Tiktaalik) display an interesting trend in the evolution of the spiracle, which is: Could they have been breathing through their spiracles? We see this today in the basal actinopterygian Polypterus.
    A review by Clack, 2007, maintains that this was an adaptation to air breathing, in effect, through the ears. Indeed, the ability of creatures like Tiktaalik to do "pushups" may have been to get the spiracles clear of the water's surface. Arguably, this was an adaptation to unusually low O2 concentrations during the Frasnian age of the Late Devonian, during which elpistostegalians radiated. Recent geochemical analyses indicate that this evolutionary pulse coincided with an interval of low O2 concentrations. This, Clack argues, stimulated the evolution of air-breathing adaptations. Naturally, creatures with the ability to elevate their heads above water to breathe, by supporting their body weight on their limbs would have the best shot at leaving the water altogether, if only for brief intervals.

    Link to additional info for all of your Tiktaalik needs.



    Acanthostega gunnari by D. Bogdanov from New Dinosaurs
    Acanthostega gunnari (Latest Devonian):

    Very well known from relatively complete skeletons.

    The overall impression is of a fully aquatic animal with rudimentary ability to support some body weight on fore and hindlimbs. What did it use its fingers and toes for? Maybe in walking on bottom or through underwater vegetation, or maybe not much at all. So the real question.....

    Enigma: Where did hands, feet, fingers, and toes come from and what were they good for?


    Hands and feet with digits appeared so rapidly that like jaws no recognizable intermediate exists in the fossil record. Developmental biology, however, suggests that there were at least three steps. Shubin's great contributions to evolutionary science (so far) are associated with this transition.

    Step one - the autopodium: In aquatic choanates, each non-terminal segment of the limb axis is followed by two elements, the next axial segment, and a preaxial (in front of the axis) radial branch. The result is:

    shown in:
    1. Cladoselache (a primitive chondrichthyan)
    2. Neoceratodus (the living Australian lungfish)
    3. Sauripteris (a primitive sarcopterygian)
    4. Panderichthys (a choanate)
    5. Tulerpeton (a stegocephalian)
    In Panderichthys (D) this is reduced to a very simple form. The limb axis is coded by HOX gene D-11 (light shading in f and g), the radials by HOX gene D-13 (dark shading in f and g). What is lacking is the hand or foot - the autopodium.

    Schematics F and G show the expression of the HOX genes in the embryonic limb buds of zebra-fish (with no autopodium) and land vertebrates (with an autopodium) respectively. Significantly the domains of the HOX D-11 and HOX D-13 genes are reversed at the end of the land vertebrate limb - yielding an autopodium.


    Step two - the digits: But just having an autopodium doesn't automatically give us digits. More recent work by Davis et al. 2007 has shown that the paddlefish Polyodon - a primitive actinopterygian - also has reversed HOX D-11 and HOX D-13 domains. Of course, it lacks digits. Woltering et al. 2014 demonstrated that in land vertebrates the expression of the HOX D genes is promoted in the proximal and distal ends of the limb bud by additional genes: promotors that are absent in fish. The combination of HOX genes and promotors results in the elongation of of skeletal elements proximal to the wrist and distal to it.

    The result:


    Step three - stopping the digits:

    The digital arch: The autopodial portion of the limb axis is called the digital arch. In vertebrates with both:

    the distal digital arch elements bifurcate into digits.

    Just as nothing prevented the lungfish from having may bifurcations between axial and postaxial elements, nothing limits the number of digital arch bifurcations to five. The number and identity of digits results from interactions of Sonic hedgehog and HOX B-8. That interaction was fine-tuned over tens of millions of years. The first stegocephalians with digits had up to eight digits. Only in the Carboniferous did the number of fingers and toes stabilize at five (four fingers for lissamphibians.)

    What happened to the fin rays? Good question. So far, all fossil stegocephalians have either fin rays or digits on their paired limbs, but never both.


    Ichthyostega stensioi
    Ichthyostega (Latest Devonian):

    Very well known (even in popular culture of previous generations) from relatively complete skeletons, but subject to much reinterpretation during the 20th century.


    Romer's Gap - a geologic enigma: Acanthostega and Ichthyostega lived roughly 365 mya. The earliest known members of the lineages leading to Lissamphibia and Amniota are from roughly 335 mya. This doesn't mean there weren't plenty of critters. For some reason, fewer were preserved as fossils or paleontologists haven't found the correct rocks. (Note: a similar contemporaneous gap exists for fossil insects.) In between there are hardly any good fossils of stegocephalians, so we are in the dark about how quickly vertebrates actually used their hands and feet to get out of the water. Even after Romer's Gap ended, most stegocephalians remained aquatic with weak limbs and prominent lateral line systems. Examples:

    All of these show ancestral characters indicting aquatic habits as adults:



    Pederpes finneyae from Palaeos.
    The first "walker?": In 2002, Jennifer Clack described Pederpes finneyae, from the middle of Romer's Gap at 350 mya. Although it retains a tiny sixth finger, has a robust lateral line system and heavy hyomandibula/stapes; it also has robust limbs and a skull that is compressed from side-to-side like early land vertebrates. We don't know how much time it spent on land, but it seems to have been able to walk. Indeed, the description of a specimen with a healed broken limb bone demonstrates that it was out of the water enough that falls were a hazard.