Proteinaceous Pheromone Affecting Female Receptivity in a Terrestrial Salamander

Abstract

A 22-kilodalton protein was isolated from the submandibular (mental) gland of the male terrestrial salamander, Plethodon jordani (family: Plethodontidae). This proteinaceous pheromone, termed plethodontid receptivity factor (PRF), was experimentally delivered to the female during courtship and shown to increase female receptivity. In most plethodontid salamanders, ovulation occurs weeks or months after insemination, so the pheromone-induced change in receptivity is the only known function of PRF. The messenger RNAs corresponding to isoforms of PRF were transcribed into complementary DNA, cloned, sequenced, and shown to have homology with cytokines of the interleukin-6 family. Pheromone activity would represent a previously unrecognized function for cytokines.

The evolution of pheromonal communication

“…Male salamanders of the genus Plethodon (the lungless salamanders) have also been shown to use reproductive pheromones, secreting skin-borne semiochemicals which induce receptivity in females during courtship [74]. As compounds that either diffuse through water, or are secreted onto permanently moist skin (in the case of Plethodon salamanders), all of these pheromones are polar proteins or peptides which are water-soluble and thus suitable for signalling in the aquatic environment in which amphibians spend at least part of their lives (see table 1).…”

Co-option and adaptation of novel gene duplications for pheromone activity in a dusky salamander.

“…More recently, pheromones with a wide variety of behavioral effects have been identified in fish (7,8), amphibians (9)(10)(11) and mammals (12)(13)(14). In particular, male mouse urine has been shown to be involved in mediating aggressive behaviors between males (15) as well as estrus synchronization and puberty acceleration in females (12,13).…”

“…Depending on the species, the pheromones are delivered to the female either by transdermal or olfactory mechanisms (10). Olfactory delivery, present in a monophyletic group of plethodontids termed the Plethodon glutinosus group, involves the male slapping the nares of the female with his hypertrophied mental gland to deliver pheromones (10) (Figure 1).…”

“…The components in the urine responsible for these behavioral and developmental changes include volatile compounds (such as 3,4-dehydroexo-brevicomin, 2-heptanone and n-pentyl acetate) and the mouse major urinary proteins to which the volatile compounds bind. Other vertebrate pheromones include androstenone, which is produced by the domestic pig to induce a receptive mating stance in females in estrus (17); 2-methylbut-2-enal, which guides newborn rabbits to their mother's nipples to obtain milk (14); and the proteinaceous pheromones of plethodontid salamanders which increase female receptivity to mate (10).…”

“…Olfactory delivery, present in a monophyletic group of plethodontids termed the Plethodon glutinosus group, involves the male slapping the nares of the female with his hypertrophied mental gland to deliver pheromones (10) (Figure 1). This mechanism is considered to be the derived trait which evolved approximately 20 million years ago.…”