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

Granatosky, Michael C.; Ross, Callum F.

doi:10.1111/joa.13279

Cited by 7 publications

(14 citation statements)

References 105 publications

(212 reference statements)

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“…Under this model, the less rhythmic feeding systems of tetrapods reflect optimization for precise control of bite force and jaw displacement over narrow ranges of gape, with the importance of this optimization varying between mammals and other chewing vertebrates (Granatosky et al. 2019; Granatosky and Ross 2020).…”

Section: Discussionmentioning

confidence: 99%

Got rhythm? Rhythmicity differences reflect different optimality criteria in feeding and locomotor systems

et al. 2022

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Evolutionary analyses of joint kinematics and muscle mechanics suggest that, during cyclic behaviors, tetrapod feeding systems are optimized for precise application of forces over small displacements during chewing, whereas locomotor systems are more optimized for large and rapid joint excursions during walking and running. If this hypothesis is correct, then it stands to reason that other biomechanical variables in the feeding and locomotor systems should also reflect these divergent functions. We compared rhythmicity of cyclic jaw and limb movements in feeding and locomotor systems in 261 tetrapod species in a phylogenetic context.Accounting for potential confounding variables, our analyses reveal higher rhythmicity of cyclic movements of the limbs than of the jaw. Higher rhythmicity in the locomotor system corroborates a hypothesis of stronger optimization for energetic efficiency: deviation from the limbs' natural frequency results in greater variability of center of mass movements and limb inertial changes, and therefore more work by limb muscles. Relatively lower rhythmicity in the feeding system may be a consequence of the necessity to prevent tooth breakage and wear, the greater complexity of coordination with tongue movements, and/or a greater emphasis on energy storage in elastic elements rather than the kinetics of limb movement.

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Section: Discussionmentioning

confidence: 99%

Got rhythm? Rhythmicity differences reflect different optimality criteria in feeding and locomotor systems

et al. 2022

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“…Jaw muscle anatomy is constrained by the bony anatomy of the adductor chamber (Holliday & Witmer, 2007; Schumacher, 1973) and by diverse functional demands including the generation of bite force while permitting sufficient mandibular mobility (Ősi, 2014; Tseng & Wang, 2010). These constraints generally prevent the feeding apparatus from having optimal efficiency in most scenarios (Granatosky & Ross, 2020). The most efficient muscular geometry for producing high bite force using the lowest amount of jaw muscle without creating tensile joint loads would direct all of muscle force collinearly through the bite point in a single vector (Greaves, 1978).…”

Section: Introductionmentioning

confidence: 99%

“…In such a system, the moment arm of each muscle vector and the moment arm of bite force would be equal, mechanical advantage would be one, and no joint forces would be produced. Additionally, in unilateral bites, contralateral muscle force can only produce bite force by lever action, in which case the optimal muscle orientation would be dorsoventral (Granatosky & Ross, 2020). Although musculoskeletal systems in which muscle forces act farther from the jaw joint than the location where biting occurs (i.e., systems with a mechanical advantage greater than one) are possible, such systems necessarily place the jaw joints under tensile loading (Huber et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

The effects of skull flattening on suchian jaw muscle evolution

Sellers

Nieto

Degrange

et al. 2022

The Anatomical Record

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Jaw muscles are key features of the vertebrate feeding apparatus. The jaw musculature is housed in the skull whose morphology reflects a compromise between multiple functions, including feeding, housing sensory structures, and defense, and the skull constrains jaw muscle geometry. Thus, jaw muscle anatomy may be suboptimally oriented for the production of bite force. Crocodylians are a group of vertebrates that generate the highest bite forces ever measured with a flat skull suited to their aquatic ambush predatory style. However, basal members of the crocodylian line (e.g., Prestosuchus) were terrestrial predators with plesiomorphically tall skulls, and thus the origin of modern crocodylians involved a substantial reorganization of the feeding apparatus and its jaw muscles. Here, we reconstruct jaw muscles across a phylogenetic range of crocodylians and fossil suchians to investigate the impact of skull flattening on muscle anatomy. We used imaging data to create 3D models of extant and fossil suchians that demonstrate the evolution of the crocodylian skull, using osteological correlates to reconstruct muscle attachment sites. We found that jaw muscle anatomy in early fossil suchians reflected the ancestral archosaur condition but experienced progressive shifts in the lineage leading to Metasuchia. In early fossil suchians, musculus adductor mandibulae posterior and musculus pterygoideus (mPT) were of comparable size, but by Metasuchia, the jaw musculature is dominated by mPT. As predicted, we found that taxa with flatter skulls have less efficient muscle orientations for the production of high bite force. This study highlights the diversity and evolution of jaw muscles in one of the great transformations in vertebrate evolution.

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“…Jaw muscle anatomy is constrained by the bony anatomy of the adductor chamber (Schumacher, 1973;Holliday and Witmer, 2007) and by diverse functional demands such as generating force for feeding while permitting sufficient gape of the mandibles (Tseng and Wang, 2010;Ősi, 2014). These constraints generally prevent the feeding apparatus from having optimal efficiency in most scenarios (Granatosky and Ross, 2020). The most efficient muscular geometry for producing bite force would direct all of muscle force collinearly through the bite point in a single vector (Greaves, 1978).…”

Section: Introductionmentioning

confidence: 99%

“…The most efficient muscular geometry for producing bite force would direct all of muscle force collinearly through the bite point in a single vector (Greaves, 1978). Additionally, in unilateral bites, contralateral muscle force can only produce bite force by lever action, in which case the optimal muscle orientation would be dorsoventral (Granatosky and Ross, 2020). However, in amniotes (Huber, Dean and Summers, 2008), these conditions are rarely approached; instead, muscles insert closer to the joint axis than the location where biting occurs, and the mandible acts like a lever even on the working side (Hylander, 1975).…”

Section: Introductionmentioning

confidence: 99%

Function and evolution of the crocodyliform feeding apparatus

Sellers¹

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The evolution of crocodylians from their suchian ancestors represents one of the great transformations in vertebrate evolution. Modern crocodylians have flat skulls and generate high forces during feeding, but crocodylian ancestors have tall skulls and lack most of the characters that help crocodylians generate and resist high forces. Thus, the evolution of crocodylians involved a substantial reorganization of the feeding apparatus. Although changes to skull shape in the lineage leading to crocodylians have received a great deal of attention, the functional consequences of shape change on feeding biomechanics are unclear. This dissertation addresses this gap in our knowledge by building high-fidelity biomechanical models to ask questions about the evolution of skull shape and feeding performance in the lineage leading from early suchians to extant crocodylians. I use detailed 3D muscle attachment sites to estimate muscle forces and distribute forces on 3D finite element models using an approach validated against in vivo data. These finite element models are used to estimate bite and joint forces. I use traditional linear morphometrics to characterize skull flattening. I also develop novel methods to quantify and visualize joint articular surface shape. These results are analyzed using phylogenetic comparative methods and ancestral character state reconstruction. My results show that skull flatness is linked with inefficient muscle geometries and that these geometries developed stepwise in the lineage leading to crocodylians. I found that joint shape best reflects the highest-magnitude loads that the skull experiences, that the orientation of joint loading tracks with skull flatness, and that peak joint pressure falls within the range predicted by chondral modeling. This study shows that extant crocodylians rely on extra muscle mass to produce high bite force with inefficient muscle configurations and that the derived, suturally-immobilized cranial joints are key features of the feeding apparatus that mitigate mechanical inefficiencies imposed by a flat skull. Overall, these results depict a coordinated evolution of skull shape, muscle anatomy, joint surface shape, and biomechanical performance in the lineage leading to Crocodylia and have broad implications and applicability to all vertebrate musculoskeletal systems. This dissertation research represents an important step in improving our understanding of the biomechanics of musculoskeletal transitions.

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

Cited by 7 publications

References 105 publications

Got rhythm? Rhythmicity differences reflect different optimality criteria in feeding and locomotor systems

Got rhythm? Rhythmicity differences reflect different optimality criteria in feeding and locomotor systems

The effects of skull flattening on suchian jaw muscle evolution

Function and evolution of the crocodyliform feeding apparatus

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