Nervous and Sensory Systems in Sub-Arctic and Antarctic Snailfishes of the Genus Paraliparis (Teleostei: Scorpaeniformes: Liparidae)
Scorpaeniform fishes of the family Liparidae (snailfishes) are anatomically distinctive, morphologically variable, ecologically diverse, and globally distributed. Liparids have both boreal and austral centers of diversity; they are one of the most speciose fish families in the North Pacific Ocean, and are the most speciose fish family in the Antarctic Southern Ocean. In a previous communication we described the nervous and sensory systems of Paraliparis devriesi from the Ross Sea of Antarctica. Our goal with the present communication is to expand and generalize these findings by examining the nervous and sensory systems of two North Pacific/sub-Arctic species, P. pectoralis and P. ulochir, which live along the northwestern coast of North America and in the Bering Sea. We find that the brains and sensory systems of all three species are grossly similar, more similar to each other than to species outside the family. These brains are derived. In response to the cold and dark conditions of the deep sea, species of Paraliparis have an augmented olfactory system, a large cephalic lateral line system, an enhanced trunk somatosensory system, and an enlarged motor coordination (cerebellar) system. But they also have a reduced, rod-only visual system, a highly reduced trunk lateral line system, and have lost some portion of the higher order processing networks for these systems (in the tectum, telencephalon, and inferior lobes). It is these reductions that give the overall impression (confirmed by outgroup comparison) that the brains of these species are comparatively small. The genus Paraliparis represents a successful evolutionary lineage by the criteria of both species diversity (106 currently described species) and distribution (global, among deep-sea [>200 m] marine environments). This evolutionary success appears to be tied to the ability to inhabit the deep-sea, the world's largest living space. For Paraliparis, the loss of brain mass is one tradeoff for occupying the world's largest habitable space and the evolutionary advantages this confers.Abstract
Lateral views of (A) two Paraliparis pectoralis and (B) Paraliparis ulochir showing overall morphology, eye size, and nostril position. Note the black peritoneum in P. pectoralis, the silver peritoneum in P. ulochir. Size ranges of P. pectoralis in our sample were 147 to 160 mm TL; P. ulochir ranged from 99 to 112 mm TL. Photos by J. Orr.
Brain of Paraliparis devriesi (TL = 180 mm) in left lateral and dorsal views. Abbreviations: CC, crista cerebellaris of the rhombencephalon; CCb, corpus division of the cerebellum; EG, eminentia granularis division of the cerebellum; Ha, habenula; IL, inferior lobe of the diencephalon; LLant, anterior lateral line nerve; LLpost, posterior lateral line nerve; nP, preoptic nucleus of the diencephalon; OB, olfactory bulb; Pit, pituitary gland; SN, spinal nerve; SON, spino-occipital nerve; Sps, spinal sensory nucleus; Sv, saccus vasculosus; Tec, tectum of the mesencephalon; Tel, telencephalon; I, olfactory nerve; II, optic nerve; III, oculomotor nerve; IV, trochlear nerve; V, trigeminal nerve; VI, abducens nerve; VII, facial nerve; VIII, auditory/vestibular nerve; IX, glossopharyngeal nerve; X, vagus nerve; Xs, visceral sensory division of the vagus nerve. Modified from Eastman and Lannoo (1998).
Histological sections of the brain of Paraliparis. (A, D, G, J) P. devriesi; cresyl violet acetate. (B, E, H, K) P. pectoralis; hematoxylin and eosin. (C, F, I, L) P. ulochir; hematoxylin and eosin. (A, B, C) Sections through the diencephalon demonstrating subependymal expansions. (D, E, F) Sections comparing midbrain tectums. (G, H, I) Sections comparing rostral medullas including corpus cerebelli. (J, K, L) Sections showing the enlarged spinal sensory nuclei (somatosensation) at the junction of the medulla and spinal cord (scale bars = 300 μm). Abbreviations: CC, crista cerebellaris of the rhombencephalon; CCb, corpus division of the cerebellum; CP, central posterior nucleus of the thalamus; Ha, habenula; Hd, dorsal division of the periventricular hypothalamic region; Hv, ventral division of the periventricular hypothalamic region; IL, inferior lobe of the diencephalon; MLF, medial longitudinal fasciculus; nP, preoptic nucleus; Pit, pituitary gland; RF, reticular formation; Sps, spinal sensory nucleus; SV, saccus vasculosus; Tec, tectum of the mesencephalon; Ts, torus semicircularis of the mesencephalon; Vm, ventromedial nucleus of the thalamus; III/IV, mesencephalic oculomotor complex.
The brain of the lumpfish, Cyclopterus lumpus, a representative cyclopterid, sister group of the liparids (from Garman, 1892). Abbreviations: CC, crista cerebellaris of the rhombencephalon; CCb, corpus division of the cerebellum; IL, inferior lobe of the diencephalon; OB, olfactory bulb; Pit, pituitary gland; Sps, spinal sensory nucleus; SV, saccus vasculosus; Tec, tectum of the mesencephalon; Tel, telencephalon; I, olfactory nerve.
Contributor Notes
Associate Editor: J. F. Webb.