Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

Abstract

How do stunning functional innovations evolve from unspecialized progenitors? This puzzle is particularly acute for ultrafast movements of appendages in arthropods as diverse as shrimps [1], stomatopods [2], insects [3-6], and spiders [7]. For example, the spectacular snapping claws of alpheid shrimps close so fast (∼0.5 ms) that jetted water creates a cavitation bubble and an immensely powerful snap upon bubble collapse [1]. Such extreme movements depend on (1) an energy-storage mechanism (e.g., some kind of spring) and (2) a latching mechanism to release stored energy quickly [8]. Clearly, rapid claw closure must have evolved before the ability to snap, but its evolutionary origins are unknown. Unearthing the functional mechanics of transitional stages is therefore essential to understand how such radical novel abilities arise [9-11]. We reconstructed the evolutionary history of shrimp claw form and function by sampling 114 species from 19 families, including two unrelated families within which snapping evolved independently (Alpheidae and Palaemonidae) [12, 13]. Our comparative analyses, using micro-computed tomography (microCT) and confocal imaging, high-speed video, and kinematic experiments with select 3D-printed scale models, revealed a previously unrecognized "slip joint" in non-snapping shrimp claws. This slip joint facilitated the parallel evolution of a novel energy-storage and cocking mechanism-a torque-reversal joint-an apparent precondition for snapping. Remarkably, these key functional transitions between ancestral (simple pinching) and derived (snapping) claws were achieved by minute differences in joint structure. Therefore, subtle changes in form appear to have facilitated wholly novel functional change in a saltational manner. VIDEO ABSTRACT.

Beyond power amplification: latch-mediated spring actuation is an emerging framework for the study of diverse elastic systems

“…Some fluidic latches can be detected as a pressure increase prior to movement followed by a rapid decrease once movement begins (Singh et al, 2011). Geometric latches can be inferred by demonstrating shifts in mechanical advantage or the direction of torques that occur during different phases of movement (Astley and Roberts, 2014;Kaji et al, 2018;Longo et al, 2018).…”

Obituary: Tomonari Kaji (1982–2019), evolutionary morphologist extraordinaire

“…Many of Tomonari's publications, on an impressive array of arthropod forms, show the great value of this two‐pronged approach for understanding the developmental or evolutionary origins of some fascinating morphological innovations, for example: A highly unusual sensory structure derived from the fusion of multiple setae in ostracods (Kaji & Tsukagoshi, ), the spectacular developmental transformation of a jointed mouthpart into a fully‐formed suction disc in branchiuran fish lice (Figure ; Kaji, Møller, & Tsukagoshi, ), transformation of body plates to yield an equally striking adhesive disk for host‐attachment in ectoparasitic copepods (Kaji et al, ), an utterly remarkable squirting head where mandibular muscles took over control of squirting as the mandibles were lost entirely in nasutitermine termite soldiers (Figure ; Kaji, Keiler, Bourguignon, & Miura, ), transformation of mandible form from simple particle‐processing to piercing carnivory in Viper copepods (Kaji et al, ), and his magisterial survey of joint morphology and muscle re‐alignment in caridean shrimp claws (Figure ; Kaji, Anker, Wirkner, & Palmer, ). The latter revealed a wholly novel energy storage mechanism for rapid claw closure that set the stage for the evolution of the spectacularly fast closing claws in snapping shrimp.…”

“…The true power of Tomonari's approach is epitomized in his magnum opus on shrimp claw morphology, function, and evolution (Figure ; Kaji et al, ). He shared my fascination with shrimp claws in those taxonomic groups within which the ability to snap loudly evolved.…”

“…At the 2016 Canadian Society of Zoologists meeting in London, Ontario (Canada), he received the President's Award for the best postdoctoral student talk. His talk was the first public presentation of results on the repeated evolutionary transitions from simple pinching claws to spectacular snapping claws in shrimp, later published in Current Biology (Kaji et al, ). During that talk, except for occasional hushed murmurs of wonder about particularly striking slides, the auditorium—which was filled with several hundred attendees—was so quiet you could hear a pin drop.…”

“…During his early postdoctoral years, Tomonari also made forays into philosophy (Kaji, 2012a(Kaji, , 2012bKaji, 2013). For example, he explained to me how he believed that the emergence of form during development was conceptually equivalent to the emergence of an idea during human Many of Tomonari's publications, on an impressive array of arthropod forms, show the great value of this two-pronged approach for understanding the developmental or evolutionary origins of some fascinating morphological innovations, for example: A highly unusual sensory structure derived from the fusion of multiple setae in ostracods (Kaji & Tsukagoshi, 2008), the spectacular developmental transformation of a jointed mouthpart into a fully-formed suction disc in branchiuran fish lice (Figure 2; Kaji, Møller, & Tsukagoshi, 2011), transformation of body plates to yield an equally striking adhesive disk for host-attachment in ectoparasitic copepods (Kaji et al, 2012), an utterly remarkable squirting head where mandibular muscles took over control of squirting as the mandibles were lost entirely in nasutitermine termite soldiers (Figure 3; Kaji, Keiler, Bourguignon, & Miura, 2016), transformation of mandible form from simple particle-processing to piercing carnivory in Viper copepods (Kaji et al, 2019), and his magisterial survey of joint morphology and muscle re-alignment in caridean shrimp claws (Figure 4; Kaji, Anker, Wirkner, & Palmer, 2018). The latter revealed a wholly novel energy F I G U R E 2 Schematic illustration of ontogeny of the first maxilla of a branchiuran crustacean (fish louse) as it transforms from a normal leg-like appendage with a hook in the early larvae (a) through to a fully functional suction disc with a distal podomere vestige in the attached juvenile (c; fig.…”