Three-dimensional limb joint mobility in the early tetrapod Ichthyostega

Abstract

The origin of tetrapods and the transition from swimming to walking was a pivotal step in the evolution and diversification of terrestrial vertebrates. During this time, modifications of the limbs—particularly the specialization of joints and the structures that guide their motions—fundamentally changed the ways in which early tetrapods could move. Nonetheless, little is known about the functional consequences of limb anatomy in early tetrapods and how that anatomy influenced locomotion capabilities at this very critical stage in vertebrate evolution. Here we present a three-dimensional reconstruction of the iconic Devonian tetrapod Ichthyostega and a quantitative and comparative analysis of limb mobility in this early tetrapod. We show that Ichthyostega could not have employed typical tetrapod locomotory behaviours, such as lateral sequence walking. In particular, it lacked the necessary rotary motions in its limbs to push the body off the ground and move the limbs in an alternating sequence. Given that long-axis rotation was present in the fins of tetrapodomorph fishes, it seems that either early tetrapods evolved through an initial stage of restricted shoulder and hip joint mobility or that Ichthyostega was unique in this respect. We conclude that early tetrapods with the skeletal morphology and limb mobility of Ichthyostega were unlikely to have made some of the recently described Middle Devonian trackways.

Massive increase in visual range preceded the origin of terrestrial vertebrates

“…Our discovery that the evolution of larger eye sockets occurred in animals that were primarily aquatic is in line with other critical conclusions of the past several decades of early tetrapod paleontology, which has found that robust limbs evolved in primarily aquatic animals (9,10) and that fingers and toes evolved in primarily aquatic animals (11). Notably, the increase in eye size starting in the elpistostegalians coincided with a distinct change in the placement of eyes in this group.…”

“…This big increase in eye size was likely driven by aquatic tetrapods surfacing their eyes above the water line and hunting like crocodiles. This lifestyle caused "primarily aquatic" features to be retained (9,11,68), while more and more robust limbs gradually evolved, enabling forays onto land (69). Because small adjustments to optical mechanics evolved to account for the change in the refractive index of air from water, there was an ever-expanding domain of visual awareness, leading these animals to long-range viewing and hunting of the bounty of invertebrate food on the shores.…”

Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

“…The sequence of character transformations in the pectoral appendicular skeleton that accompanied the fins-to-limbs and water-to-land transitions in tetrapods has been described in detail (e.g. Coates, Jeffery & Ruta, 2002;Shubin, Daeschler & Coates, 2004;Hall, 2008;Boisvert, 2009;Callier, Clack & Ahlberg, 2009;Ahlberg, 2011;Pierce, Clack & Hutchinson, 2012). Changes between tetrapodomorph fish such as Eusthenopteron and Devonian tetrapods such as Acanthostega include the following: in the shoulder girdle, dermal bones spanning the head-trunk boundary were lost and the endoskeletal girdle was enlarged (Coates et al, 2002;, and the orientation of the shoulder joint (glenoid) changed from posterior to posterolateral.…”

“…The radius and ulna transformed from flattened, diverging elements of unequal length to two parallel cylinders articulating distally with multiple carpal bones (Andrews & Westoll, 1970a;Ahlberg, 2011 skeleton lost its dermal fin rays (lepidotrichia) and gained digits. Functionally, these changes led to the pectoral limb becoming a weight-bearing appendage directed laterally rather than posteriorly (Boisvert, Mark-Kurik & Ahlberg, 2008) with restricted shoulder rotation Pierce et al, 2012;Pierce, Hutchinson, & Clack, 2013), and a flexed elbow (Ahlberg, 2011). Reconstructions of soft tissue anatomy are equally important as those of the skeleton because they can provide crucial information about locomotion, mode of life, and ecology of extinct animals (Witmer, 1995).…”

The origins, scaling and loss of tetrapod digits

“…While the evolutionary mechanism remains controversial, it is thought that the origin of the autopod lies early within Sarcopterygii where homologies to a modern digit bearing autopod can be seen in Devonian stem tetrapods, Acanthostega and Ichthyostega, that appeared around 360 Ma [27][28][29][30]. Like their predecessors, these species were probably entirely aquatic as their limbs lacked flexion at the joints that would be later required for supporting body weight on land [31].…”