Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes

Abstract

Tetrapods evolved from sarcopterygian fishes in the Devonian and were the first vertebrates to colonize land. The locomotor component of this transition can be divided into four major events: terrestriality, the origins of digited limbs, solid substrate-based locomotion, and alternating gaits that use pelvic appendages as major propulsors. As the sister group to tetrapods, lungfish are a morphologically and phylogenetically relevant sarcopterygian taxon for understanding the order in which these events occurred. We found that a species of African lungfish (Protopterus annectens) uses a range of pelvic fin-driven, tetrapod-like gaits, including walking and bounding, in an aquatic environment, despite having a derived limb endoskeleton and primitively small, muscularly supported pelvis. Surprisingly, given these morphological traits, P. annectens also lifts its body clear of the substrate using its pelvic fins, an ability thought to be a tetrapod innovation. Our findings suggest that some fundamental features of tetrapod locomotion, including pelvic limb gait patterns and substrate association, probably arose in sarcopterygians before the origin of digited limbs or terrestriality. It follows that the attribution of some of the nondigited Devonian fossil trackways to limbed tetrapods may need to be revisited.T he vertebrate water-to-land transition initiated in the Devonian was a key event in the history of life. The ability to move in a variety of terrestrial and semiterrestrial environments opened up a range of new ecosystems for colonization and led to the diversity of tetrapod clades we see today. One essential adaptation in the evolution of tetrapods was the ability to locomote on land, a trait that required significant morphological and functional changes in the appendicular system. Many of these morphological changes can be observed in the fossil record (1-14). Work on basal tetrapod fossils has revealed that even those with digited limbs can be aquatic (5, 7). Some major questions these findings raised were how tetrapod-like limbs functioned in aquatic habitats, and in what sequence the characteristics of terrestrial tetrapod locomotion were acquired. These characteristics include the broad use of alternating limb movements, as in walking, the use of pelvic appendages as major propulsors, and the use of a bottom substrate (i.e., the solid surface underlying the fluid environment) to generate propulsive force.Whereas body fossils cannot directly inform the order in which these functional traits were acquired, fossil trackways can give us valuable information on how animals moved. Many fossil trackways from the Devonian are indicative of quadrupedal and bipedal gaits very similar to those used by modern terrestrial tetrapods (1,3,9,13,14). That tracks were preserved demonstrates that these animals were walking on a substrate. That these trackways have a cosmopolitan distribution implies that the animals responsible for generating them were themselves widespread, and likely abundant and diverse. Because we can...

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

“…Convergence in form suggests a role for common selective pressures. In tetrapods, these vertebral morphologies were thought to have evolved in response to the demands of terrestrial weight-bearing and/or limb-driven locomotion [13,14,44]. The latter scenario is challenged by the ability of lungfishes and other animals to walk underwater without even fully ossified centra [44].…”

“…Yet, fast swimming cannot entirely explain observed convergence: distinctive regional modifications are mostly lacking in other swimming, similarly shaped taxa (e.g. Paratarrasius, lungfishes, Arapaima) [17,25,44] (see electronic supplementary material).…”

The Relationship between Branchiosomatic and Pulmosomatic Indices in the African Lungfish, Protopterus Annectens of Anambra River, Nigeria

“…(Carroll, ISSN 2157-6076 2014 www.macrothink.org/jbls 138 1997; King et al, 2011). The amphibians have two stages in their life history.…”

“…Thus, at this period, before the splitting of Pangaea, an extinct Crossopterygian group related to modern lungfish evolved into amphibians and eventually all tetrapods (Randall et al, 1981;Brinkmann et al, 2004;Shan and Gras, 2011). This helps to explain the homology between many organs of lungfish with those of amphibians, indicating a closer relationship between these two groups than can be revealed by palaeontological or other physiological or genetic studies (King et al, 2011;Shan and Gras,2011).…”

“…The Devonian period or the Age of Fishes was a time of violent alternation of seasons (Caroll, 1997;Ahlberg et al, 2003;King et al, 2011;Shan and Gras, 2011). There were wet seasons alternating with times of severe drought (Randall et al, 1981;Carroll, 1997).…”