Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes - PubMed (original) (raw)

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

Heather M King et al. Proc Natl Acad Sci U S A. 2011.

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Alternating and synchronous pelvic fin gaits in P. annectens. A and B illustrate two bouts of bipedal locomotion. Angles are 2D and are relative to the body wall. An angle of 0° indicates that the fin is adducted in the direction of the head; an angle of 180° indicates adduction in the direction of the tail; an angle of 90° indicates that the fin is perpendicular to the body wall. Fin contacts with the substrate are indicated by an x or *. (A) Alternating pelvic fin gait (x steps); duration 8.48 s. (B) Alternating pelvic fin gait, with a discrete transition to a synchronous pelvic fin gait (* steps); duration 11.18 s.

Fig. 2.

Fig. 2.

Fin angles and duty factors for benthic gaits in P. annectens. A and C correspond to Fig. 1_A_, and B and D correspond to Fig. 1_B_. (A) Alternating pelvic fin gait and (D) corresponding duty factor. (B) Alternating pelvic fin gait with discrete transition to a synchronous pelvic fin gait and (C) corresponding duty factor. In A and B, note the lack of rhythmic movement in the pectoral fin angles. (E) Duty factor summary for a single step cycle in a terrestrial tetrapod (Dicamptodon tenebrosus); error bars are SEM. LH, left hindlimb; LF, left forelimb; RH, right hindlimb; RF, right forelimb. Reproduced with permission from the Journal of Experimental Biology (24).

Fig. 3.

Fig. 3.

Lifting of body and fins clear of the substrate and range of rotation of pelvic fins in P. annectens. (A) Movie stills in lateral view. (B) Outline of lateral-view movie stills to emphasize the location of the fins and body. (C) Corresponding ventral view. Note that P. annectens can lift its body clear of the substrate, and that the pelvic fin moves dorsally and rostrally relative to the articulation with the body. Here we show a generalized step cycle: (D) lateral view, (E) ventral view, and (F) three-quarter view. See text for peak angles in each direction. Note that these angles were measured at the base of the fin, and do not represent the trajectory of the entire fin. The range of movement of the pelvic fins allows the animal to lift both its fins and body clear of the substrate during benthic movement.

Fig. 4.

Fig. 4.

Location of lungs and center of mass in P. annectens. The location of the lungs relative to the pelvic fins (PF) and center of mass (COM) suggests that the air-filled lungs would allow the pelvic fins to both propel the fish and lift its body clear from the bottom. The center of mass was located at 35.8 ± 1.7% of total body length, and the pelvic fins were located at 54.0 ± 2.5% of total body length. Lung location was redrawn from Owen (18). Center of mass and pelvic fin location (means and SD) were taken from n = 9 individuals.

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