A Devonian tetrapod-like fish and the evolution of the tetrapod body plan

Abstract

The relationship of limbed vertebrates (tetrapods) to lobe-finned fish (sarcopterygians) is well established, but the origin of major tetrapod features has remained obscure for lack of fossils that document the sequence of evolutionary changes. Here we report the discovery of a well-preserved species of fossil sarcopterygian fish from the Late Devonian of Arctic Canada that represents an intermediate between fish with fins and tetrapods with limbs, and provides unique insights into how and in what order important tetrapod characters arose. Although the body scales, fin rays, lower jaw and palate are comparable to those in more primitive sarcopterygians, the new species also has a shortened skull roof, a modified ear region, a mobile neck, a functional wrist joint, and other features that presage tetrapod conditions. The morphological features and geological setting of this new animal are suggestive of life in shallow-water, marginal and subaerial habitats.The evolution of tetrapods from sarcopterygian fish is one of the major transformations in the history of life and involved numerous structural and functional innovations, including new modes of locomotion, respiration and hearing. Fish and tetrapod fossils across this transition can reveal how these innovations were assembled. During the origin of tetrapods in the Late Devonian (385-359 million years ago), the proportions of the skull were remodelled, the series of bones connecting the head and shoulder was lost, and the region that was to become the middle ear was modified. At the same time, robust limbs with digits evolved, the shoulder girdle and pelvis were altered, the ribs expanded, and bony connections between vertebrae developed. Few of these features, however, are seen in the closest relatives of tetrapods-the elpistostegalian fishes-which are incompletely known. Elpistostege, for example, is represented only by two partial dermal skull roofs and a segment of the axial skeleton from the early Frasnian Escuminac Formation in Quebec 1-3 . The best-known elpistostegalian, Panderichthys, consists of complete specimens of Middle to Late Devonian age (late Givetian and early Frasnian stages) mostly from the Lode quarry in Latvia 4-10 . Panderichthys possesses relatively few tetrapod synapomorphies, and provides only partial insight into the origin of major features of the skull, limbs and axial skeleton of early tetrapods. In view of the morphological gap between elpistostegalian fish and tetrapods, the phylogenetic framework for the immediate sister group of tetrapods has been incomplete and our understanding of major anatomical transformations at the fish-tetrapod transition has remained limited.The discovery of a new elpistostegalian sarcopterygian from the Fram Formation in Nunavut Territory, Canada (Fig. 1) significantly enhances our knowledge of the fish-tetrapod transition. Many articulated specimens from a single site are used to describe a taxon that is a remarkable intermediate between Panderichthys and early tetrapods. The material provides oppor...

Tetrapod-like axial regionalization in an early ray-finned fish

“…Evidence from Tarrasius and Scyliorhinus suggests a distinct cervical region is not a tetrapod-specific trait evolved through axial elongation [2,9,13,15]. In zebrafish, both the HoxC3 marker for tetrapod forelimb position and Hox4 marker for tetrapod cervical -thoracic transition are expressed behind the pectoral fin origin [1,16,18].…”

“…In zebrafish, both the HoxC3 marker for tetrapod forelimb position and Hox4 marker for tetrapod cervical -thoracic transition are expressed behind the pectoral fin origin [1,16,18]. If an elongated, Hox-defined cervical region is ancestral for vertebrates, then it would be likely that the shoulder girdle simply moved relative to this series during tetrapod evolution, rather than becoming separated from the skull through axial elongation [15,16,22]. However, it is important to note that all the above interpretations depend on the assumption that the same general Hox domains related to specific vertebral regions in all vertebrates.…”

“…Even the origin of the tetrapod body plan has been linked to clade-specific elongation of the trunk and related changes in the placement of nested Hox expression domains [9,13,14]. The process was capped by the appearance of a flexible, distinct neck (cervical region) and the evolution of a distinct sacrum in early tetrapods and their relatives [13][14][15][16][17]. Regional distinctions, many involving reinforcement of the axial column, arose in multiple tetrapod lineages from the Devonian (416-359 Ma) onwards and are widely considered to be an adaptation to terrestrial lifestyles [14].…”

The Concept of Co-option: Why Evolution Often Looks Miraculous

“…The bones of the upper and forearm, wrist, hand, and rudimentary fingers all evolved in a fin-like structure supplemented with thin, bony rods called lepidotrichia that plesiomorphically provided support for the fin. Functional analysis indicates that the newest member of the tetrapod family tree, Tiktaalik Daeschler et al 2006), could have propped itself up on these arm-fins and used them to move along the bottom and margins of the rivers and streams in which it lived . Tetrapods themselves are characterized by the loss of the lepidotrichia, giving the fin its new "limb" look, the appearance of complex, articulated fingers, possibly allowing the animals to maneuver through shallow, vegetationrich water (Retallack 2004).…”

The pectoral fin of Panderichthys and the origin of digits

“…These can tentatively be interpreted as attributes of the 'elpistostegid' segment of the tetrapod stem lineage and thus ancestral for the tetrapod forelimb. Given that recent phylogenies consistently place Panderichthys below Tiktaalik in the tetrapod stem group 19,20 , it is surprising to discover that its pectoral fin skeleton is more limb-like than that of its supposedly more derived relative. In Tiktaalik 4 , like in 'osteolepiforms' 17 and rhizodonts 18 (more primitive fish members of the stem group), the ulna and ulnare are of similar size.…”