Developing the Snapping Shrimp, Alpheus angulosus, as a Model System for Development and Plasticity
Tracey, Erica Renee
Neural asymmetry is usually considered in the context of handedness and language processing in humans, but handedness and behavioral side preferences (reflecting asymmetry in neural organization) can be found to some degree in all vertebrate and invertebrate families. This universality suggests that lateralized specialization is a beneficial characteristic under strong evolutionary selection. Despite this, few solid conclusions have been drawn as to what bilateral asymmetry may require from the nervous system and how phenotypic differences are representative of the underlying circuitry. Other related processes, such as neural regeneration and plasticity, are also poorly understood, especially as they relate to neural asymmetry. Simple systems with extreme phenotypic characteristics, like some crustaceans, can provide a window into mechanisms associated with successful neuroplasticity, regeneration and organization of asymmetric systems that traditional model systems cannot. Like many crustaceans, those of the genus Alpheus, or snapping shrimp, present with extreme bilateral asymmetry in their front limbs. Wild type shrimp have a large hammer claw (also known as snapper) used for defense and a smaller pincer claw used to burrow and feed. These functional differences are echoed by the set of setae present on the claw surface that relay sensory input back to the central nervous system. Setae are small hairs outside the crustacean’s cuticle that are either chemo or mechanosensory in nature. These setae are diverse in form and distribution among specific regions of the claw in a single species. Studies of Alpheus heterochaelis, closely related to Alpheus angulosus, show that these setae are innervated with nerves that branch and that different types of setae may serve varied purposes. Snapping shrimp stand out from the rest of crustaceans because if one claw is removed, the “handedness” of the shrimp often becomes switched—the pincer morphing into a snapper, while the removed limb grows back as a pincer, in a process beginning as early as a week after removal. This transformation occurs in a stepwise fashion, the transforming pincer looking more like a snapper after each molt. During this transformation, the sensory hairs (setae) and internal neuromuscular system must be completely rewired to compensate for the behavioral and functional differences between the two claws. As the pincer transforms into snapper, up to 5000 myelinated and 9000 unmyelinated neurons are regenerated and send axons to synapse in the thoracic ganglion5. This process is recognized as an example of neural regeneration coupled with neural plasticity. Some work has been done to characterize how the muscles and their associated motor neurons change functionally to support the move from pincer to snapper. Almost nothing is known, however, about the significant neural reorganization that occurs in the peripheral and central nervous systems to support these radical changes in wiring. Also unique to the snapping shrimp, “handedness” appears to be random as opposed to environmentally determined or genetically preferred, as in most crustaceans. This feature suggests that snapping shrimp have evolved to optimize plasticity rather than fixed asymmetry. This ability is probably the basis for the regeneration and switching described earlier, and the randomness should be reflected during development. As such, my research group proposes to use the development of Alpheus as a model system for neural development and plasticity as it will provide significant insights into fundamental problems in neurobiology. The following compilation of papers reflects two years of data collection. We undertook a multidirectional approach to begin building the snapping shrimp as a model species, exploring both embryological development and claw form and function. The first paper, published in Crustaceana, represents the beginning of our embryological studies. It is essentially an atlas of morphological markers that we are currently using to match early neurological patterns with phenotypic characteristics. Paper two, submitted for publication in Marine and Freshwater Behavior and Physiology, analyzes changes in claw shape and function as it transforms from a small claw into a large claw. Taken together, this work forms a solid basis on which to begin understanding how deeply the neural asymmetry and plasticity of snapping shrimp is integrated into their system.
Alpheus angulosus, neuroplasticity, regeneration, development