Pheromone Gene Diversification and the Evolution of Courtship Glands in Plethodontid Salamanders.

ABSTRACT

Proteinaceous pheromones that diversify through gene duplication can result in shifts in courtship cocktails that may serve as a mechanism for reproductive isolation. The molecular evolution of pheromones has been extensively studied in salamanders, but how these genes and associated novel courtship glands have codiversified has not been evaluated. In this study we used transcriptional analyses to examine the relationship between pheromone diversification and gland type in three divergent lineages of plethodontid salamanders. Our results revealed that plethodontid salamanders express up to eight divergent Sodefrin Precursor-like Factor genes (spf, representing both alpha and beta subfamilies) along with Plethodontid Modulating Factor (pmf) and Plethodontid Receptivity Factor (prf). Expression of pheromone genes is tissue specific with pmf, prf, and some spf genes restricted to the mental gland. In contrast, the caudal gland shows strong expression of the other spf genes. We found evidence for punctuated changes in pheromone cocktail composition related to the loss of metamorphosis, and subsequent extreme reduction of the mental gland, in a paedomorphic lineage. Our study provides insight into how pheromone diversification can be partitioned into unique glands, which may lead to cocktail specificity in behavioral modules during courtship.