Feeding biomechanics in Acanthostega and across the fish-tetrapod transition

Abstract

Acanthostega is one of the earliest and most primitive limbed vertebrates. Its numerous fish-like features indicate a primarily aquatic lifestyle, yet cranial suture morphology suggests that its skull is more similar to those of terrestrial taxa. Here, we apply geometric morphometrics and two-dimensional finite-element analysis to the lower jaws of Acanthostega and 22 other tetrapodomorph taxa in order to quantify morphological and functional changes across the fish-tetrapod transition. The jaw of Acanthostega is similar to that of certain tetrapodomorph fish and transitional Devonian taxa both morphologically (as indicated by its proximity to those taxa in morphospace) and functionally (as indicated by the distribution of stress values and relative magnitude of bite force). Our results suggest a slow tempo of morphological and biomechanical changes in the transition from Devonian tetrapod jaws to aquatic/semi-aquatic Carboniferous tetrapod jaws. We conclude that Acanthostega retained a primitively aquatic lifestyle and did not possess cranial adaptations for terrestrial feeding.

Keywords: Acanthostega; feeding; finite-element analysis; fin–limb transition; geometric morphometrics; phylogeny.

Figure 1.

(a) Simplified cladogram for the 23 taxa used in this study; groups are colour-coded as follows: blue, tetrapodomorph fish; red, Devonian stem tetrapods; orange, aquatic/semi-aquatic Carboniferous stem tetrapods; green, anthracosaurs; purple, temnospondyls. (b) VM stress distribution in 28 jaw models with a muscle vector of 60°, drawn to the same length and with stress values colour-coded as in inset scale.

Figure 2.

Biomechanical performance of jaws, colour-coded as in figure 1. (a) Mean relative bite force measurements for each taxon as a proportion of Acanthostega bite force. (b) Bite ‘efficiency’ of each taxon; note the high efficiency in temnospondyl taxa despite low relative bite force. For taxa with more than one model and thus efficiency value, the mean was used. (c) Mean relative bite force as a proportion of Acanthostega bite force, plotted against mean VM stress; numbers correspond to taxa shown in (a) and (b); note the linear relationship between stress and bite force, except for the outlying positions of Megalocephalus and Rhizodus. BF, bite force.

Figure 3.

Plot of principal components 1 and 2, which account for 68.08% of the total morphological variance; colour key is the same as in figure 1; Ichthyostega 80 is from [50] and Ichthyostega 96 is from [51]. Inset shows the jaw of Acanthostega, redrawn from [23], with the position of the 12 landmarks used in the morphometric analysis (landmark descriptions can be found in the electronic supplementary material, table S3).