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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
- 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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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz104
