Chemistry Between Salamanders: Evolution of the SPF Courtship Pheromone System in Salamandridae

Chemical communication is an important aspect of courtship and reproduction in salamanders (Urodela), where males secrete several protein pheromones from various sexually dimorphic glands. The most widely used sex pheromone system consists of proteins of the Sodefrin Precursor-like Factor (SPF) family. This protein family already started diversifying through gene duplications in the Late Palaeozoic and continued to do so in various urodelan lineages. As a result, males of multiple extant salamander species secrete different sets or ratios of SPF protein pheromones which, as shown in behavioral tests, can evoke various female responses during the courtship process, such as following behavior, cloacal gaping, or an acceleration of courtship in general. Still, all observable effects essentially are a consequence of female receptivity enhancement, indicating a preserved role for SPF pheromones. Salamandridae is a large family with currently 119 described species that show a considerable variety in courtship behaviour. In this family, different lineages evolved various modes of pheromone transfer, ranging from direct application during amplexus on land, to an indirect transfer in which males abandoned physical contact and instead tail-fan pheromones underwater toward a nearby female. In one genus, an additional decapeptide pheromone, sodefrin, originated by cleavage from a precursor of the SPF family and was co-opted alongside uncleaved SPF protein pheromones. Here we discuss our current understanding and knowledge gaps on the use of the SPF pheromone system in salamandrids, and we define some testable hypotheses on its evolution in relation to changes in mating habitat and courtship modes.