Modularity and Scaling in Fast Movements: Power Amplification in Mantis Shrimp

Abstract

Extremely fast animal actions are accomplished with mechanisms that reduce the duration of movement. This process is known as power amplification. Although many studies have examined the morphology and performance of power-amplified systems, little is known about their development and evolution. Here, we examine scaling and modularity in the powerful predatory appendages of a mantis shrimp, Gonodactylaceus falcatus (Crustacea, Stomatopoda). We propose that power-amplified systems can be divided into three units: an engine (e.g., muscle), an amplifier (e.g., spring), and a tool (e.g., hammer). We tested whether these units are developmentally independent using geometric morphometric techniques that quantitatively compare shapes. Additionally, we tested whether shape and several mechanical features are correlated with size and sex. We found that the morphological regions that represent the engine, amplifier, and tool belong to independent developmental modules. In both sexes, body size was positively correlated with the size of each region. Shape, however, changed allometrically with appendage size only in the amplifier (both sexes) and tool (males). These morphological changes were correlated with strike force and spring force (amplifier), but not spring stiffness (amplifier). Overall, the results indicate that each functional unit belongs to different developmental modules in a power-amplified system, potentially allowing independent evolution of the engine, amplifier, and tool. K E Y W O R D S :Geometric morphometrics, raptorial appendage shape, scaling, Stomatopoda, strike force.Fast biological movements fascinate biologists for their remarkable biomechanical designs and behavioral feats. Studies of these systems have formed the foundation of a field focused on power amplification-the mechanism by which organisms reduce the time to perform a movement (Alexander and Bennet-Clark 1977; Alexander 1983); however, little attention has been given to the evolution of their morphology. Studies of the modular organization of organisms have brought fundamental insights to the understanding of the development and evolution of traits and organs

Giant Australian cuttlefish use mutual assessment to resolve male-male contests

“…For many taxa, the outcome of animal contests is influenced by body size 447 (Haley, Deutsch, & Le Boeuf, 1994;Wells, 1988) because this attribute is generally 448 correlated with strength and the ability to inflict injury (Archer, 1988;Parker, 1974). For 449 example, in mantis shrimp, Gonodactylaceus falcatus, larger individuals have a physical 450 advantage over smaller individuals because both spring and strike force of the raptorial attack 451 are correlated positively with body size (Claverie, Chan, & Patek, 2011). 452…”

Mechanical sensitivity and the dynamics of evolutionary rate shifts in biomechanical systems

“…Previous work by Claverie & Patek [31] examined rates of morphological disparity across mantis shrimp raptorial segments using composite, geometric morphometrics measurements that reflected the interdependence (modularity) of changes in size and shape across the segments (e.g. [60,61]). They found that disparity accumulated more quickly in spearers than in smashers.…”

Studying morphological integration and modularity at multiple levels: concepts and analysis

“…An intraspecific analysis found that the functional subdivision into engine, amplifier and tool also corresponds to the pattern of developmental integration, where those three elements form separate modules [55]. A comparative analysis across the clade showed that the tool behaves as an evolutionary module separate from engine and amplifier [26].…”

“…An excellent example of a study that links functional considerations to developmental and evolutionary integration is the analysis of variation in the predatory appendages of mantis shrimp [26,55]. An intraspecific analysis found that the functional subdivision into engine, amplifier and tool also corresponds to the pattern of developmental integration, where those three elements form separate modules [55].…”

“…Because fluctuating asymmetry originates from random variation in developmental processes, the asymmetries of different traits are correlated only if there are direct interactions between developmental pathways that produce the traits [46,47]. This approach has been applied in a broad range of animal systems [10,[12][13][14][15]27,36,37,[48][49][50][51][52][53][54][55]. Whereas this reasoning applies widely to motile organisms, including most animals, caution is necessary in applying it to sessile organisms like most plants, where a part of fluctuating asymmetry may be due to plastic responses to heterogeneity in microenvironmental factors [25,56].…”