Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

Tomonari Kaji; Arthur Anker; Christian S Wirkner; A Richard Palmer

doi:10.1016/j.cub.2017.11.044

Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

Curr Biol. 2018 Jan 8;28(1):106-113.e4. doi: 10.1016/j.cub.2017.11.044. Epub 2017 Dec 28.

Authors

Tomonari Kaji¹, Arthur Anker², Christian S Wirkner³, A Richard Palmer⁴

Affiliations

¹ Systematics and Evolution Group, Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada; Universität Rostock, Institut für Biowissenschaften, Allgemeine & Spezielle Zoologie, Universitätsplatz 2, 18055 Rostock, Germany; Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, BC V0R 1B0, Canada. Electronic address: flickloop@gmail.com.
² Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus Samambaia, ICB-5, Avenida Esperança s/n, Goiânia, GO 74690-900, Brazil.
³ Universität Rostock, Institut für Biowissenschaften, Allgemeine & Spezielle Zoologie, Universitätsplatz 2, 18055 Rostock, Germany.
⁴ Systematics and Evolution Group, Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada; Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, BC V0R 1B0, Canada.

PMID: 29290559
DOI: 10.1016/j.cub.2017.11.044

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.

Keywords: Alpheidae; Palaemonidae; biomechanics; comparative morphology; evo-devo; evolutionary morphology; functional morphology; innovation; saltational evolution; torque-reversal joint.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Biological Evolution*
Biomechanical Phenomena
Decapoda / anatomy & histology*
Hoof and Claw / anatomy & histology*
Movement
Palaemonidae / anatomy & histology
Phylogeny
X-Ray Microtomography