Unique Osmoregulatory Morphology in Primitive Sharks: An Intermediate State Between Holocephalan and Derived Shark Secretory Morphology

Discovery of an unusual rectal gland in the Atlantic sixgill shark, Hexanchus vitulus, led to examination of rectal glands in 29 species of epipelagic and deep-sea sharks. Eight of 14 deep-sea species of sharks had digitiform glands that were previously assumed to be characteristic of elasmobranchs (N=281; mean width-length ratio ± SD = 0.18 ± 0.07). Hematoxylin-and-eosin stained sections from deep-sea sharks were similar to those from shallow water sharks. Glands from the family Somniosidae were kidney bean-shaped (N = 3; mean width-length ratio ± SD = 0.46 ± 0.05); whereas those from the families Echinorhinidae and Hexanchidae appeared lobulate (N=39; mean width-length ratio ± SD = 0.58 ± 0.11). Histology of hexanchid rectal glands showed a morphology characterized by smooth muscle dividing the tubules into sections around a lumen. Rectal gland width-length ratios were significantly different among eight species with digitiform morphology and two hexanchids (ANOVA; R2=0.86; df=14, 292; F=125.01; P\u3c0.001). The significant plasma constituents, urea and TMAO, followed the piezolyte hypothesis and were highest in deep-sea sharks with the exception of Cl-, which was highest in species with lobulate rectal glands. This study represents the first histology of the unique rectal gland morphology in Hexanchus sp., and it suggests that the distinct gland morphology seen in species of Hexanchidae and Echinorhinidae is a plesiomorphic trait and is not characteristic of deep-sea sharks as a group. Interestingly, the similarities between lobulate rectal glands and the secretory morphology of holocephalans may represent a secretory morphology intermediate between that of Holocephali and derived shark species