The mystery of the two-unit skull of the Sarcopterygii: a trap for functional morphologists

Abstract

This is an analytical study which presents a rigorous biomechanical interpretation of the well known but poorly understood two-unit skull of extant Latimeria and extinct non-dipnoan sarcopterygian fishes. The two units, anterior ethmosphenoid and posterior otoccipital, are hinged, dorsally, by intracranial syndesmosis between parietal and postparietal bones of the skull roof, and interconnected, centrally, by intracranial segment of the notochord and, ventrally, by a very strong paired subcephalic muscle unique to these fishes. This muscle depresses the anterior unit with the upper jaw, and this movement is kinematically coupled, in Latimeria, with the mandible elevation and, in basal sarcopterygians, with narrowing of the jaws and the oropharyngeal cavity. However, the muscular antagonist able to raise the anterior unit was never found. Neither manipulations on thawed Latimeria nor modern techniques of CT scanning and computer modeling helped to solve the puzzle. To find the way out, researchers were forced to rely, implicitly, on various fantastic mechanisms, such as strut-like action of ligaments, positive mechanical work of elongating muscles, mechanical force action without opposite reaction and depression of the snout without elevation, etc. An accurate analysis of statics of the head of Latimeria shows that all of the most important muscles (m. subcephalicus, m. levator arcus palatini, m. coracomandibularis and m. adductor mandibulae) are synergists in respect of snout depression. I suggest a new idea that their antagonist, which is only possible, is parietal musculature acting via notochord. Indeed, the longitudinal contraction of the trunk myomeres causes some shortening of postcranial segment of the notochord, and consequently, forward protrusion of its liquid-filled intracranial segment. Thus, the last pushes, as a hydraulic drive, the anterior skull unit. The problem is posed, whether the cranial muscles depressing the snout are able to counteract the pressure force in the notochord produced by powerful parietal musculature during undulatory swimming of the fish. Otherwise, the skull mechanism could be broken. Calculation of physiological cross-sectional areas of major muscles involved allows to state that the m. subcephalicus is strong enough to counteract myomeric contraction. In basal sarcopterygians, the m. adductor mandibulae did not yet participate in this struggle because the hyomandibular suspension of the jaws was not shifted from the jaw joint onto the retroarticular process of the mandible. The biomechanic-based explanation is suggested of how this shift could occur gradually in the evolution of coelacanths. The second novelty of Latimeria and its relatives, the forward shift of the intracranial syndesmosis relative to the notochordal apex, is explained too, as a means to engage ligamentous suspension of the intracranial notochord under prootic bones in stopping the snout elevation under the pressure of the notochord. The new idea on adaptive significance of the neurocranial kinesis of sarcopterygian fishes is suggested: this mechanism allows the recruitment of powerful parietal musculature into prey suction with water by oropharyngeal expansion.