The feeding system of Tiktaalik roseae : an intermediate between suction feeding and biting

Abstract

Changes to feeding structures are a fundamental component of the vertebrate transition from water to land. Classically, this event has been characterized as a shift from an aquatic, suction-based mode of prey capture involving cranial kinesis to a biting-based feeding system utilizing a rigid skull capable of capturing prey on land. Here we show that a key intermediate, Tiktaalik roseae, was capable of cranial kinesis despite significant restructuring of the skull to facilitate biting and snapping. Lateral sliding joints between the cheek and dermal skull roof, as well as independent mobility between the hyomandibula and palatoquadrate, enable the suspensorium of T. roseae to expand laterally in a manner similar to modern alligator gars and polypterids. This movement can expand the spiracular and opercular cavities during feeding and respiration, which would direct fluid through the feeding apparatus. Detailed analysis of the sutural morphology of T. roseae suggests that the ability to laterally expand the cheek and palate was maintained during the fish-to-tetrapod transition, implying that limited cranial kinesis was plesiomorphic to the earliest limbed vertebrates. Furthermore, recent kinematic studies of feeding in gars demonstrate that prey capture with lateral snapping can synergistically combine both biting and suction, rather than trading off one for the other. A “gar-like” stage in early tetrapod evolution might have been an important intermediate step in the evolution of terrestrial feeding systems by maintaining suction-generation capabilities while simultaneously elaborating a mechanism for biting-based prey capture.

Osteology and digital reconstruction of the skull of the early tetrapod Whatcheeria deltae

“…In summary, sutural morphology in the skull and lower jaws of Whatcheeria supports a feeding mode whereby prey was initially seized by biting using enlarged anterior teeth, with vertical forces generated being directed through the anterior snout to the skull roof (and through the adsymphysials and dentaries to the posterior lower jaw). Early tetrapods and their relatives likely utilized a combination of suction-feeding and direct biting, as exemplified by the transitional, gar-like feeding system of Tiktaalik roseae (Lemberg et al, 2021). The shift from suction to biting across the water-to-land transition therefore appears to be a gradual one, with taxa falling somewhere along a spectrum rather than as two distinct functional categories.…”

A Permian fish reveals widespread distribution of neopterygian-like jaw suspension

“…The anterior process of the parasphenoid, anterior to the orbitosphenoid region of the braincase, exhibits a posterodorsally-anteroventally directed groove on each side (apal, Figure 5A, C, F, G and H ). These grooves either transmitted the parabasal canals or were employed in the articulation of the palate, as in, for example, polypterids and sarcopterygians ( Lemberg et al, 2021 ).…”

The neuroecology of the water-to-land transition and the evolution of the vertebrate brain

“…The transitional tetrapods, some of which are believed to have been primarily aquatic such as Tiktaalik, already show this adaptation [28]. Given the flattening of the skull with eyes perched high (figure 2) and the use of biting for predation [29] in addition to the more common suction method found in aquatic animals, these animals appear to already be exploiting a greater visual range. What they used this for is less clear, but seeing distant prey over the water surface would have been possible, including terrestrial invertebrates (preceding vertebrates on to land by 50 Ma), other transitional tetrapods and air-breathing fishes [30] that surfaced to breathe using ventilation holes just behind the eyes (spiracles, green; figure 2), or early amphibious taxa and stranded fishes [2,27,31,32].…”