Joint angular excursions during cyclical behaviors differ between tetrapod feeding and locomotor systems

Abstract

Tetrapod musculoskeletal diversity is usually studied separately in feeding and locomotor systems. However, comparisons between these systems promise important insight into how natural selection deploys the same basic musculoskeletal toolkitconnective tissues, bones, nerves and skeletal muscleto meet the differing performance criteria of feeding and locomotion. In this study, we compare average joint angular excursions during cyclic behaviorschewing, walking and runningin a phylogenetic context to explore differences in the optimality criteria of these two systems. Across 111 tetrapod species, average limb-joint angular excursions during cyclic locomotion are greater and more evolutionarily labile than those of the jaw joint during cyclic chewing. We argue that these findings reflect fundamental functional dichotomies between tetrapod locomotor and feeding systems. Tetrapod chewing systems are optimized for precise application of force over a narrower, more controlled and predictable range of displacements, the principal aim being to fracture the substrate, the size and mechanical properties of which are controlled at ingestion and further reduced and homogenized, respectively, by the chewing process. In contrast, tetrapod limbed locomotor systems are optimized for fast and energetically efficient application of force over a wider and less predictable range of displacements, the principal aim being to move the organism at varying speeds relative to a substrate whose geometry and mechanical properties need not become more homogeneous as locomotion proceeds. Hence, the evolution of tetrapod locomotor systems has been accompanied by an increasing diversity of limbjoint excursions, as tetrapods have expanded across a range of locomotor substrates and environments.

Evolution of the speech‐ready brain: The voice/jaw connection in the human motor cortex

“…It is this mandibular cycling that provides the “frame” for the syllable, whereas movements of the other oral articulators (the lips, tongue, and soft palate) contribute to the “content” that determines the specific character of the phoneme (e.g., ma vs. ba). Interestingly, mandibular cycling is not just conserved between humans and nonhuman primates, but seems to be a stable physiological feature of all tetrapods (Granatosky et al, 2019).…”

Differences in muscle mechanics underlie divergent optimality criteria between feeding and locomotor systems

“…To explore optimality criteria of the feeding and locomotor systems, Granatosky et al (2019) compared average joint angular excursions during cyclic behaviors-chewing, walking, and running-in a comparative phylogenetic context across 111 tetrapod species.…”

“…Taken together, small variations in the anatomical configuration of muscle moment arms, mechanical advantage, and force vector orientation can have profound effects on the mechanics of a system. As such, a comparative analysis of these variables between the feeding and locomotor systems should serve as a powerful tool to either support or refute the hypothesis regarding differences in optimality criteria proposed by Granatosky et al (2019). Specifically, if the feeding system is optimized for precise application of high forces and the locomotor system is optimized for broad and rapid joint excursions for minimal muscle activation, then it is likely that (a) the moment arms of the jaw elevator muscles should be relatively large and close to maximum throughout the range of jaw excursion compared to flexor and extensor musculature of the limbs; (b) the mechanical advantage of jaw elevators should be greater than those of flexor and extensor musculature of the limbs; and (c) the orientation F I G U R E 1 Changes in muscle moment arm lengths (a and b) and muscle force vector orientations relative to the resistance arm (c and d) at the jaw (a and c) and elbow (b and d) joints between maximum gape/elbow extension (left) and minimum gape/elbow flexion (right) of the jaw elevator muscles relative to the resistance arm should be more orthogonal through the range of jaw excursion compared to flexor and extensor musculature of the limbs.…”

“…For example, diversity in feeding‐system morphology has been related to variation in feeding behavior and diet in a wide range of vertebrates, including fish, birds, lizards, and mammals (Westneat, 2004; Reilly and McBrayer, 2007; Olsen, 2017), and diversity in locomotor morphology has been linked to variation in locomotor mode, ecology, substrate preference, and overall habitat (Garland and Losos, 1994; Higham, 2007; Reilly et al ., 2007; Fabre et al ., 2017). In contrast, studies that explicitly compare the two systems are much less common, despite the insight they provide into general principles of musculoskeletal design (English, 1985; Higham, 2007; Ross et al ., 2017; Ahn et al ., 2018; Granatosky et al ., 2019; Olsen, 2019; Anderson and Roberts, 2020).…”

Testing the propulsive role of m. peroneus longus during quadrupedal walking in Varanus exanthematicus

“…However, this arrangement is usually only present in species in which the crus and pes maintain a relatively anteroposterior orientation relative to the travel path (e.g., mammals and crocodilians) (Bassarova, Janis, & Archer, 2009; Brinkman, 1980a; Giddings, Beaupre, Whalen, & Carter, 2000; Ginot, Hautier, Marivaux, & Vianey‐Liaud, 2016; Su, Skedros, Bachus, & Bloebaum, 1999). For sprawling lizards, the highly abducted hindlimb and lateral rotation of the crus relative to the pes results in a kinematic arrangement in which the ankle plantarflexors are not in line with the travel path at the end of stance phase (Brinkman, 1980b; Foster & Higham, 2012; Granatosky et al, 2019a; Irschick & Jayne, 1999; Reilly, 1995; Sullivan, 2010). Instead, Sullivan (2010) recognized that some sprawling tetrapods (e.g., varanids, proterosuchids, erythrosuchids, Euparkeria , and proterochampsids) show a prominent and highly distinctive lateral calcaneal process, and posited that this structure serves as a lateral “heel” to increase the moment arm for m. peroneus longus.…”