Unique osmoregulatory morphology in primitive sharks: an intermediate state between holocephalan and derived shark secretory morphology

• Published in: Journal of fish biology Vol. 95; no. 5; pp. 1331 - 1341
• Main Authors: Larsen, Matthew E., Abel, Daniel C., Crane, Derek P., Parker, Scott L., Yancey, Paul H., Keller, Bryan A., Grubbs, Dean R.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.11.2019; Wiley Subscription Services, Inc
• Subjects: Adaptation, Physiological; Animals; Atlantic sixgill shark; Biological Evolution; deep sea; Ecosystem; Electrolytes; Glands; Hexanchidae; Hexanchus; Histology; Kidney beans; Length; Marine fishes; Morphology; Muscles; Organic chemistry; Osmoregulation; Phylogeny; Physical characteristics; Plasma chemistry; Rectal gland; Rectum; Seafood; secretory; Sharks; Sharks - anatomy & histology; Sharks - physiology; Smooth muscle; Species; Species diversity; Trimethylamine; Urea; Variance analysis; Width; Atlantic sixgill shark; histology; Hexanchidae; deep sea; rectal gland; secretory; Hexanchus
• ISSN: 0022-1112; 1095-8649
• DOI: 10.1111/jfb.14139

Discovery of an unusual rectal gland in the Atlantic sixgill shark Hexanchus vitulus led us to examine the rectal glands of 31 species of sharks to study diversity in rectal‐gland morphology. Twenty‐four of 31 species of sharks had digitiform glands (mean width–length ratio ± SD = 0.17 ± 0.04) previously assumed to be characteristic of all elasmobranchs regardless of habitat depth or phylogenetic age. Rectal glands from the family Somniosidae were kidney bean‐shaped (mean width: length ± SD = 0.46 ± 0.05); whereas those from families Echinorhinidae and Hexanchidae were lobulate (mean width: length ± SD = 0.55 ± 0.06). Rectal gland width: length were different among species with digitiform morphology and lobulate morphology (ANOVA; R2 = 0.9; df = 15, 386; 401, F = 219.24; P < 0.001). Histological and morphological characteristics of the digitiform morphology from deep‐sea sharks were similar to those from shallow‐water sharks. Histology of lobulate rectal glands from hexanchids were characterised by tubule bundles separated by smooth muscle around a central lumen. Additionally, we examined plasma chemistry of four species of sharks with digitiform rectal glands and two species with lobulate rectal‐gland morphology to see if there were differences between morphologies. Plasma chemistry analysis showed that urea and trimethylamine N‐oxide (TMAO) followed the piezolyte hypothesis, with TMAO being highest and urea being lowest in deep‐sea sharks. Among electrolytes, Na+ was highest in species with lobulate rectal glands. Hexanchids and echinorhinids both have lobulate rectal glands similar to those of holocephalans, despite the more than 400 million years separating these two groups. The morphological similarities between the lobulate rectal‐gland anatomy of primitive sharks and the secretory morphology of holocephalans may represent an intermediate state between Holocephali and derived shark species.