Abstract Animals use a diverse array of motion to feed, escape predators, and reproduce. Linking morphology, performance, and fitness is a foundational paradigm in organismal biology and evolution. Yet, the influence of mechanical relationships on evolutionary diversity remains unresolved. Here, I focus on the many-to-one mapping of form to function, a widespread, emergent property of many mechanical systems in nature, and discuss how mechanical redundancy influences the tempo and mode of phenotypic evolution. By supplying many possible morphological pathways for functional adaptation, many-to-one mapping can release morphology from selection on performance. Consequently, many-to-one mapping decouples morphological and functional diversification. In fish, for example, parallel morphological evolution is weaker for traits that contribute to mechanically redundant motions, like suction feeding performance, than for systems with one-to-one form–function relationships, like lower jaw lever ratios. As mechanical complexity increases, historical factors play a stronger role in shaping evolutionary trajectories. Many-to-one mapping, however, does not always result in equal freedom of morphological evolution. The kinematics of complex systems can often be reduced to variation in a few traits of high mechanical effect. In various different four-bar linkage systems, for example, mechanical output (kinematic transmission) is highly sensitive to size variation in one or two links, and insensitive to variation in the others. In four-bar linkage systems, faster rates of evolution are biased to traits of high mechanical effect. Mechanical sensitivity also results in stronger parallel evolution—evolutionary transitions in mechanical output are coupled with transition in linkages of high mechanical effect. In other words, the evolutionary dynamics of complex systems can actually approximate that of simpler, one-to-one systems when mechanical sensitivity is strong. When examined in a macroevolutionary framework, the same mechanical system may experience distinct selective pressures in different groups of organisms. For example, performance tradeoffs are stronger for organisms that use the same mechanical structure for more functions. In general, stronger performance tradeoffs result in less phenotypic diversity in the system and, sometimes, a slower rate of evolution. These macroevolutionary trends can contribute to unevenness in functional and lineage diversity across the tree of life. Finally, I discuss how the evolution of mechanical systems informs our understanding of the relative roles of determinism and contingency in evolution.
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Extending the Geometric Approach for Studying Biomechanical Motions
Abstract Whether it is swimming, walking, eating, or jumping, motions are a fundamental way in which organisms interact with their environment. Understanding how morphology contributes to motion is a primary focus of kinematic research and is necessary for gaining insights into the evolution of functional systems. However, an element that is largely missing from traditional analyses of motion is the spatial context in which they occur. We explore an application of geometric morphometrics (GM) for analyzing and comparing motions to evaluate the outputs of biomechanical linkage models. We focus on a common model for oral jaw mechanics of perciform fishes, the fourbar linkage, using GM to summarize motion as a trajectory of shape change. Two traits derived from trajectories capture the total kinesis generated by a linkage (trajectory length) and the kinematic asynchrony (KA) of its mobile components (trajectory nonlinearity). Oral jaw fourbar data from two subfamilies of Malagasy cichlids were used to generate form–function landscapes, describing broad features of kinematic diversity. Our results suggest that kinesis and KA have complex relationships with fourbar morphology, each displaying a pattern in which different shapes possess equivalent kinematic trait values, known as many-to-one mapping of form-to-function. Additionally, we highlight the observation that KA captures temporal differences in the activation of motion components, a feature of kinesis that has long been appreciated but was difficult to measure. The methods used here to study fourbar linkages can also be applied to more complex biomechanical models and broadly to motions of live organisms. We suggest that they provide a suitable alternative to traditional approaches for evaluating linkage function and kinematics.
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- Award ID(s):
- 1839250
- NSF-PAR ID:
- 10170994
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 3
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 684 to 695
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (
Anas platyrhynchos ; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro‐computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate‐articular); otic joint (quadrate‐squamosal); palatobasal joint (parasphenoid‐pterygoid); the mandibular symphysis (dentary‐dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution. -
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ABSTRACT The extinct nonavian dinosaur
Tyrannosaurus rex , considered one of the hardest biting animals ever, is often hypothesized to have exhibited cranial kinesis, or, mobility of cranial joints relative to the braincase. Cranial kinesis inT .rex is a biomechanical paradox in that forcefully biting tetrapods usually possess rigid skulls instead of skulls with movable joints. We tested the biomechanical performance of a tyrannosaur skull using a series of static positions mimicking possible excursions of the palate to evaluate Postural Kinetic Competency inTyrannosaurus . A functional extant phylogenetic bracket was employed using taxa, which exhibit measurable palatal excursions:Psittacus erithacus (fore–aft movement) andGekko gecko (mediolateral movement). Static finite element models ofPsittacus ,Gekko , andTyrannosaurus were constructed and tested with different palatal postures using anatomically informed material properties, loaded with muscle forces derived from dissection, phylogenetic bracketing, and a sensitivity analysis of muscle architecture and tested in orthal biting simulations using element strain as a proxy for model performance. Extant species models showed lower strains in naturally occurring postures compared to alternatives. We found that fore–aft and neutral models ofTyrannosaurus experienced lower overall strains than mediolaterally shifted models. Protractor muscles dampened palatal strains, while occipital constraints increased strains about palatocranial joints compared to jaw joint constraints. These loading behaviors suggest that even small excursions can strain elements beyond structural failure. Thus, these postural tests of kinesis, along with the robusticity of other cranial features, suggest that the skull ofTyrannosaurus was functionally akinetic. Anat Rec, 303:999–1017, 2020. © 2019 Wiley Periodicals, Inc. -
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ABSTRACT Billfishes are large pelagic fishes that have an extreme elongation of the upper jaw bones forming the rostrum. Recent kinematic and biomechanical studies show the rostrum to be associated to feeding, however, it is less clear how the wide range of morphologies present among billfish may affect their striking behavior. In this study, we aim to assess the mechanical performance of different rostrum morphologies under loads that simulate feeding and to test existing hypotheses of species‐specific feeding behaviors. We use finite element analysis (FEA)—a physics‐based method that predicts patterns of stress and strain in morphologically complex structures under specified boundary conditions—to test hypotheses on the form and mechanical performance of billfish rostra. Patterns of von Mises stress and total strain energy suggest that distinct rostral morphologies may be functionally segregated. The rounder blue marlin rostrum may be better suited for a wide range of slashing motions to disable prey, whereas the more flattened swordfish rostrum appears to be more specialized for lateral swiping during prey capture. The almost homogenous stress distribution along each rostrum implies their possible use as a predatory weapon regardless of morphological differences between species. The mechanical implications of other less commonly reported behaviors such as spearing are discussed, as well as the potential impact of hydrodynamics in shaping the evolution of the rostrum in this lineage. Anat Rec, 2019. © 2019 American Association for Anatomy.
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Synopsis The concept of modularity is fundamental to understanding the evolvability of morphological structures and is considered a central framework for the exploration of functionally and developmentally related subsets of anatomical traits. In this study, we explored evolutionary patterns of modularity and integration in the 4-bar linkage biomechanical system of the skull in the fish family Labridae (wrasses and parrotfishes). We measured evolutionary modularity and rates of shape diversification of the skull partitions of three biomechanical 4-bar linkage systems using 205 species of wrasses (family: Labridae) and a three-dimensional geometric morphometrics data set of 200 coordinates. We found support for a two-module hypothesis on the family level that identifies the bones associated with the three linkages as being a module independent from a module formed by the remainder of the skull (neurocranium, nasals, premaxilla, and pharyngeal jaws). We tested the patterns of skull modularity for four tribes in wrasses: hypsigenyines, julidines, cheilines, and scarines. The hypsigenyine and julidine groups showed the same two-module hypothesis for Labridae, whereas cheilines supported a four-module hypothesis with the three linkages as independent modules relative to the remainder of the skull. Scarines showed increased modularization of skull elements, where each bone is its own module. Diversification rates of modules show that linkage modules have evolved at a faster net rate of shape change than the remainder of the skull, with cheilines and scarines exhibiting the highest rate of evolutionary shape change. We developed a metric of linkage planarity and found the oral jaw linkage system to exhibit high planarity, while the rest position of the hyoid linkage system exhibited increased three dimensionality. This study shows a strong link between phenotypic evolution and biomechanical systems, with modularity influencing rates of shape change in the evolution of the wrasse skull.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz104
