Independently evolved toad-eating snakes exhibit sexually dimorphic enlargement of adrenal glands

Authors


  • We dedicate this paper to the memory of Hobart M. Smith, who died on 4 March 2013 at the age of 100. His pioneering observations on enlargement and sexual dimorphism of the adrenal glands of Heterodon served as the inspiration for our work. Dr. Smith's generous mentorship of one of the authors (A. H. S.) is gratefully acknowledged.
  • Editor: Mark-Oliver Rödel

Correspondence

Alan H. Savitzky, Department of Biology, Utah State University, Logan, Utah 84322-5305, USA. Tel: +1 435 797 1909; Fax: +1 435 797 0532.

E-mail: savitzky@usu.edu

Abstract

Toads are defended chemically by bufadienolides, a class of cardiotonic steroids lethal to most predators. Bufadienolides bind to Na+,K+-ATPases, inhibiting the ability of those cellular pumps to transport ions. In cardiocytes, this inhibition causes arrhythmia and increased contractile strength, which, if prolonged, lead to death. However, several snakes are resistant to bufadienolides and consume toads with no apparent ill effects. Adrenal glands produce hormones that function in the maintenance of Na+,K+-ATPases, and may therefore play an important role in countering the negative effects of bufadienolides. We hypothesized that bufophagous (toad-eating) snakes have enlarged adrenal glands that contribute to the snakes' resistance to bufadienolides, and that sexual dimorphism in adrenal gland size is a general characteristic of bufophagous snakes. We compared phylogenetically independent pairs of taxa to investigate differences in adrenal morphology between bufophagous and nonbufophagous species. We also compared adrenal masses between males and females of bufophagous and nonbufophagous species to test whether sexual dimorphism in adrenal size reported for one species of bufophagous snakes represents a more widespread phenomenon. Our results demonstrate for the first time that the allometric relationship between adrenal mass and body size is significantly different between several bufophagous species and related nonbufophagous species; adrenal size differs between males and females in those bufophagous species, with males having larger adrenal glands, but no such dimorphism exists in related nonbufophagous species. These results demonstrate that parallel morphological responses have occurred repeatedly in bufophagous snakes and suggest that the adrenal glands play a role in mediating the negative effects of bufadienolide ingestion in bufophagous snakes.

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