Competing influences on morphological modularity in biomechanical systems: a case study in mantis shrimp

Abstract

Related species that share similar biomechanical systems and segmentation patterns may exhibit different patterns of morphological covariation. We examined morphological covariation of the potent prey capture appendage of two mantis shrimp (Stomatopoda) species-a spearer (Squilla empusa) and smasher (Gonodactylaceus falcatus). We assessed three frameworks for modularity, two based on the biomechanics of the appendage and one based on its segmentation as a proxy for shared developmental pathways. We collected morphometric data from S. empusa, and compared morphological covariation patterns across the raptorial appendage with patterns from a new analysis of previously published morphometric data from G. falcatus. The relative importance of the different hypothetical influences differed between the two species, and was dependent on whether specimens were analyzed all together or subdivided based on sex or sub-populations, including one particularly distinct population in the Gulf of Mexico. We also found an intriguing handedness pattern in which right-hand appendages had a variable number of spines, whereas the left had a constant number of spines. Overall, our findings highlight the importance of testing multiple, alternative frameworks for morphological covariation and suggest that mantis shrimp experience contrasting influences on covariation depending on their feeding mechanisms.

Rates of morphological evolution, asymmetry and morphological integration of shell shape in scallops

“…This would suggest that the two valves are closely associated during development and share the same gene regulatory pathways [ 81 ]. The strength of covariation between parts of articulated morphological structures would be much lower than what we observed here if the two valves are evolving as separate ‘modules’, for example in mammalian limbs [ 40 , 41 ] and mantis shrimp claws [ 82 , 83 ]. We propose that high evolutionary integration in scallop shells across all species is the result of a functional constraint for the hinge elements and shape of the commissural margin between left and right valves to interlock.…”

Evolutionary Integration and Modularity in the Archosaur Cranium

“…The differences across these groups in patterns of integration and modularity and integration are largely concentrated on the structures that form the palate and cranio-mandibular joint(s). This result adds to the growing body of evidence that patterns of integration are largely conserved within major clades but they are not immutable and can evolve (Goswami 2006;Piras et al 2014;Haber 2015;Anderson et al 2016;Heck et al 2018). Because these groups differ so greatly in cranial disparity, geometry, mechanics, and development, a key next step is to investigate the causes of these shifts in trait correlations.…”

“…Patterns of integration and modularity are thought to evolve (Wagner and Altenberg 1996;Goswami et al 2015). However, most studies of evolutionary modularity have focused on single clades and do not assess shifting patterns of trait correlation (although see Goswami 2006;Piras et al 2014;Haber 2015;Anderson et al 2016;Heck et al 2018). The tetrapod skull has been one of the most common structures used to studying phenotypic modularity.…”

The principles of cascading power limits in small, fast biological and engineered systems

“…Only a few studies and systems have been examined in the context of tuning and integration to achieve power amplification. The mantis shrimp's motor, spring, and projectile coevolved as integrated components (87)(88)(89)(90)(91), such that species producing the greatest accelerations evolved springs with greater work capacity and muscles with force-modified architecture at the expense of contraction velocity. They evolved with varying degrees of integration (i.e., correlated change among components): More tightly integrated components are associated with greater acceleration and spring work but with slower accumulation of change over evolutionary time (89).…”