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.2015 Apr 7;282(1804):20143088.
doi: 10.1098/rspb.2014.3088.

Mechanical sensitivity reveals evolutionary dynamics of mechanical systems

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Mechanical sensitivity reveals evolutionary dynamics of mechanical systems

P S L Anderson et al. Proc Biol Sci..

Abstract

A classic question in evolutionary biology is how form-function relationships promote or limit diversification. Mechanical metrics, such as kinematic transmission (KT) in linkage systems, are useful tools for examining the evolution of form and function in a comparative context. The convergence of disparate systems on equivalent metric values (mechanical equivalence) has been highlighted as a source of potential morphological diversity under the assumption that morphology can evolve with minimal impact on function. However, this assumption does not account for mechanical sensitivity-the sensitivity of the metric to morphological changes in individual components of a structure. We examined the diversification of a four-bar linkage system in mantis shrimp (Stomatopoda), and found evidence for both mechanical equivalence and differential mechanical sensitivity. KT exhibited variable correlations with individual linkage components, highlighting the components that influence KT evolution, and the components that are free to evolve independently from KT and thereby contribute to the observed pattern of mechanical equivalence. Determining the mechanical sensitivity in a system leads to a deeper understanding of both functional convergence and morphological diversification. This study illustrates the importance of multi-level analyses in delineating the factors that limit and promote diversification in form-function systems.

Keywords: biomechanics; evolution; mechanical equivalence; mechanical sensitivity.

© 2015 The Author(s) Published by the Royal Society. All rights reserved.

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Figures

Figure 1.
Figure 1.
Examining the mechanical sensitivity of a mechanical metric to variation in its morphological components is key to understanding the evolutionary dynamics of mechanically equivalent systems, such as a four-bar linkage. (a) Mechanical equivalency occurs when multiple morphological configurations yield convergent values of a mechanical metric, such as kinematic transmission (KT). (b) Mechanical sensitivity is indicated by variable effects of components on the mechanical metric, such that some are tightly correlated to the metric (L1, red) and others are not correlated (L2, orange; L3, blue). Thus, in this example, the evolutionary diversification of KT is influenced by the component to which it is most sensitive (L1), whereas components to which KT is less sensitive (L2 and L3) are free to diversify without affecting KT. Combining analyses of mechanical equivalence with analyses of mechanical sensitivity can provide a more accurate portrait of the evolutionary dynamics of form–function relationships than is offered by analyses at only the mechanical equivalence level. (Online version in colour.)
Figure 2.
Figure 2.
The raptorial appendage of the mantis shrimp (Stomatopoda) is a spring-driven, power-amplified appendage used to strike prey items at ultra-fast speeds (peak speeds up to 30.6 m s−1, accelerations up to 154 km s−2) [24,25]. (a) A smasher mantis shrimp,Neogonodactylus bredini, is holding the raptorial appendage in a folded position (black outline). (b) Smashers use the hammer-shaped base of the dactyl to break open hard-shelled prey. (c) Spearers snag softer, evasive prey with an elongate, spiny dactyl. (d) Force and motion generated by the spring mechanism are transferred to the swinging appendage via a four-bar linkage. The meral-V rotates distally (to left of page) when the spring is released. This action pushes on the swinging arm, which then rotates distally to perform the strike. (e) Mechanical equivalence was measured using discrete landmarks (red dots) that represent the morphology of the whole four-bar linkage system. (f) Mechanical sensitivity of individual components was measured via individual link lengths (coloured and numbered lines). Scale bars, 15 mm. Distal, left; dorsal, top of the page. (Online version in colour.)
Figure 3.
Figure 3.
The stomatopod linkage system shows the classic pattern of mechanical equivalence in which a mechanical metric (KT; colour map) is overlaid onto a morphospace based on linkage morphology. The morphospace is composed of PC axes 1 and 2 from a landmark-based PC analysis of 195 stomatopod specimens (each point represents an individual specimen). A total of 36 species are represented with 1–10 specimens per species. KT is overlaid onto the morphospace as a ‘heat map’ showing a pattern of decoupled KT from morphology. Three ecological groups defined by appendage mechanics (smashers, spearers and undifferentiated) are identified in morphospace and show overlap in morphology and KT. (Online version in colour.)
Figure 4.
Figure 4.
By examining the mechanical sensitivity of the stomatopod four-bar system, it is possible to identify the influence of individual morphological components on the evolution of mechanical outputs. (a) Plots of kinematic transmission (KT) versus the overall morphology of the four-bar system, denoted here by PC axes 1–3, show a decoupling of form from function as expected in a mechanically equivalent system. (b) However, plots of KT versus the individual components of the system (the lengths of links 2, 3 and 4 all divided by link 1, as explained in the Methods) show that one component (link 3) is tightly correlated with KT, which potentially allows the other components (link 2 and link 4) to vary independently from KT. (Online version in colour.)
Figure 5.
Figure 5.
This phylomorphospace of the stomatopod linkage system illustrates the mechanically equivalent nature of kinematic transmission (KT). The morphospace is composed of PC axes 1 and 2 from a landmark-based PC analysis of 36 stomatopod species representing overall morphology of the linkage system. Previous work showed that the four-bar system in spearing clades (Lysiosquilloidea, Parasquilloidea, Pseudosquilloidea and Squilloidea; shown in colour) all evolve towards high KT values. However, this phylomorphospace indicates that each clade does so with distinctive morphologies (sometimes multiple morphologies within clades). Furthermore, certain taxa from the Parasquilloidea and Pseudosquilloidea clades inhabit morphospace adjacent to the smasher clade (Gonodactyloidea; shown in black). (Online version in colour.)
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