Terrestrial-style feeding in a very early aquatic tetrapod is supported by evidence from experimental analysis of suture morphology

Abstract

There is no consensus on when in the fish-tetrapod transition suction feeding, the primary method of prey capture in the aquatic realm, evolved into the direct biting on prey typical of terrestrial animals. Here, we show that differences in the morphology of selected cranial sutures between species that span the fish-tetrapod transition (the Devonian osteolepiform fish Eusthenopteron, the aquatic Devonian tetrapod Acanthostega, and the Permian terrestrial tetrapod Phonerpeton) can be used to infer when terrestrial feeding first appeared. Our approach consists of defining a sutural morphospace, assigning functional fields to that morphospace based on our previous measurements of suture function made during feeding in the living fish Polypterus, inferring the functions of the fossil sutures based on where they fall in the morphospace, and then using the correlation between feeding mode and the patterns of inferred suture function across the skull roof in taxa where feeding mode is unambiguous to infer the feeding mode practiced by Acanthostega. Using this procedure, we find that the suture morphologies of Acanthostega are inconsistent with the hypothesis that it captured prey primarily by means of suction, which suggests that it may have bitten directly on prey at or near the water's edge. Thus, our data strongly support the hypothesis that the terrestrial mode of feeding first emerged in aquatic taxa.

Fig. 1.

Cross-sections through the IF and IP sutures of the osteolepiform fish Eusthenopteron and their approximate positions through the skull roof (see Introduction for discussion of the terminology used for these bones). The cross-section drawings are modified after the original drawings in the literature (29). The color of the sutural label indicates the location of the slice through the skull. The dorsal reconstruction is modified from the literature (30) and was largely based on SMNH P222, the specimen used to generate the grinding series and cross-sectional drawings. [Scale bars: 1 mm (sutures) and 1 cm (skull).] Fr, frontal; Pa, parietal.

Fig. 2.

Photographs and camera lucida drawings of selected midline and coronal sutures in the aquatic Devonian tetrapod Acanthostega. The midline IF, IP, and IPP sutures were observed in coronal sections of MGUH f.n. 236. The NF and FP sutures were observed in MGUH f.n. 1305 (sectioned sagittally). The black arrows indicate the endocranial and ectocranial emergence of each suture. The colored bar on the top of each suture photograph indicates the approximate position of that slice through the skull roof of Acanthostega. Slices whose positions are shown in black on the dorsal reconstruction of Acanthostega were measured in this study but are not figured here. Note the dramatic shape changes within the IP and IPP sutures. [Scale bars: 1 mm (suture) and 1 cm (skull).] The dorsal reconstruction of the skull of Acanthostega is modified from the literature (31). Na, nasal; Fr, frontal; Pa, parietal; PPa, postparietal; L NF, left nasofrontal suture; L FP, left frontoparietal suture.

Fig. 3.

Cropped CT slices and line drawings of selected midline and coronal sutures in the Permian terrestrial tetrapod Phonerpeton and their positions in the skull roof. The white and black arrows indicate the ecto- and endocranial ends of each suture in cross-section. [Scale bars: 1 mm (suture) and 1 cm (skull).] The colored line across the top of each CT image indicates the position of that slice in the skull. Slices whose positions are shown in black on the dorsal reconstruction of Phonerpeton were measured in this study but are not figured here. The CT slices were obtained from Phonerpeton specimen MCZ 1414. Note the obvious shape change within the IPP suture. The dorsal reconstruction at left has been modified from the literature (24). Fr, frontal; Pa, parietal; PPa, postparietal; Na, nasal; R NF, right nasofrontal; R FP, right frontoparietal.

Fig. 4.

Sutural morphospace defined by cross-sectional sutural measurements in Eusthenopteron, Acanthostega, and Phonerpeton. The volumes defined by suture morphologies in the extant fish Polypterus known to experience tension, compression, or a combination of tension and compression that reflects more complex loading conditions (such as shearing or bending) are shown in pink, blue, and green, respectively. The locations of the fossil data points within these volumes are used to infer the loading conditions experienced by the fossil sutures. Taxa: Polypterus, purple; Eusthenopteron, blue; Acanthostega, red; Phonerpeton, green. Sutures: IF, ●; IP, ■; IPP, ♦; left frontoparietal (LFP), ◀; right frontoparietal (RFP), ▶; left nasofrontal (LNF), ▴; right nasofrontal (RNF), ▾. (Scale bars: 1 mm.)

Fig. 5.

Inferred strain patterns in the skulls of Eusthenopteron, Acanthostega, and Phonerpeton based on sutural morphology. Strain patterns observed in the extant fish Polypterus (23) are included for comparison. The strain pattern inferred for Acanthostega suggests that it may have been capable of feeding on land, although Acanthostega may also have occasionally captured prey by means of suction in the aquatic realm. Dorsal view reconstructions are modified from published illustrations: Polypterus (26), Eusthenopteron (30), Phonerpeton (24), and Acanthostega (31). See Figs. 1–3 for suture morphologies and bone labels.