The Anatomical Distribution Patterns, Physiological Effects, and Quantification of Biogenic Amines in the Central Nervous Systems of Araneae and Scorpiones (Arthropoda: Chelicerata)

Abstract

The arthropod subphylum Chelicerata is one of the most diverse groups of organisms on the planet, and yet relatively little is known about the structural and functional organization of chelicerate central nervous systems (CNSs). To address this knowledge gap, I conducted a comparative study of biogenic amines in the CNSs of three representative chelicerates: the wolf spider Hogna lenta (Araneae: Lycosidae), the jumping spider Phidippus regius (Araneae: Salticidae), and the bark scorpion Centruroides sculpturatus (Scorpiones: Buthidae). In H. lenta and P. regius, I mapped the anatomical distribution of catecholaminergic neurons (i.e., those that produce dopamine [DA] or norepineprhine [NE]) in the CNS, using an antiserum against tyrosine hydroxylase (TH), the rate-limiting enzyme in catecholamine synthesis. TH immunoreactivity was detected throughout the spider CNS, including in the visual system, the arcuate body (a site of sensorimotor integration), and the neuromeres of the appendages and opisthosoma, thus suggesting that catecholamines play vital roles in many different behaviors and other physiological processes in spiders. Using similar immunocytochemical methods, I also described the distribution of catecholaminergic neurons in the ventral nerve cord (VNC) of C. sculpturatus, as well as neurons that contain octopamine (OA) and serotonin (5-hydroxytryptamine, 5-HT). Of particular note in the scorpion were clusters of large efferent TH-ir neurons, which exited the CNS to directly innervate the tissues of the book lungs, implying a role for catecholaminergic modulation of respiratory functions. These studies include the first description of catecholamines in any chelicerate taxon, and provide a much-needed foundation upon which future functional studies of biogenic amines in chelicerates can be based. Additionally, I utilized a combination of immunocytochemistry, quantitative chemistry, electrophysiology, and bioinformatics techniques to examine the possibility that NE is an endogenous signaling molecule in chelicerates, despite the widespread notion that invertebrates lack NE. Using ultra-performance liquid chromatography and mass spectrometry, I detected non-trace amounts of NE in the CNSs of both C. sculpturatus and H. lenta. Endogenous NE was localized to cells of the supraneural lymphoid glands in the scorpion, which implies a previously unrecognized secretory role for these structures. NE was also shown to elicit robust patterned electrophysiological activity in the terminal nerves of the scorpion, which was distinct from the patterns produced by other amines. Finally, I identified genes for distinct NE, OA, and DA receptors in the C. sculpturatus genome. Taken together, my results support the idea that NE is an endogenous and physiologically active modulator in scorpions, and possibly in the Chelicerata more broadly, thus challenging the idea that adgrenergic signaling is exclusive to the vertebrates. The implications of these findings are discussed in relation to the evolution of aminergic systems within the Arthropoda and the Bilateria as a whole.