Abstract
Courtship is pivotal for successful mating. However, courtship is challenging for the Cryptococcus neoformans species complex, comprised of opportunistic fungal pathogens, as the majority of isolates are α mating type. In the absence of mating partners of the opposite mating type, C. deneoformans can undergo unisexual reproduction, during which a yeast-to-hyphal morphological transition occurs. Hyphal growth during unisexual reproduction is a quantitative trait, which reflects a strain’s ability to undergo unisexual reproduction. In this study, we determined whether unisexual reproduction confers an ecological benefit by promoting foraging for mating partners. Through competitive mating assays using strains with different abilities to produce hyphae, we showed that unisexual reproduction potential did not enhance competition for mating partners of the same mating type, but when cells of the opposite mating type were present, cells with enhanced hyphal growth were more competitive for mating partners of either the same or opposite mating type. Enhanced mating competition was also observed in a strain with increased hyphal production that lacks the mating repressor gene GPA3, which contributes to the pheromone response. Hyphal growth in unisexual strains also enables contact between adjacent colonies and enhances mating efficiency during mating confrontation assays. The pheromone response pathway activation positively correlated with unisexual reproduction hyphal growth during bisexual mating and exogenous pheromone promoted bisexual cell fusion. Despite the benefit in competing for mating partners, unisexual reproduction conferred a fitness cost. Taken together, these findings suggest C. deneoformans employs hyphal growth to facilitate contact between colonies at long distances and utilizes pheromone sensing to enhance mating competition.
Highlights
Successful courtship is key to the evolutionary success of sexual organisms, and many species have evolved distinct strategies to locate and choose a mating partner
We showed that the undirected hyphal growth during unisexual reproduction enables MATα cells to forage for mating partners over a larger surface area, and when MATα hyphae come into close proximity of rare MATa cells, pheromone response pathway activation in both MATα and MATa cells can further enhance mating
Strains with enhanced unisexual reproduction potential are more competitive for mating partners of the opposite mating type
Summary
Successful courtship is key to the evolutionary success of sexual organisms, and many species have evolved distinct strategies to locate and choose a mating partner. Primates and humans utilize aggression to secure a mating partner [1]; male hummingbirds apply acoustic control using tail feathers during high-speed dives to court females [2]; male Drosophila vibrate their wings to generate different songs to trigger mating responses in females [3]; male tree-hole frogs adopt acoustic strategies taking advantage of tree trunk cavities to attract females [4]; and female pipefish display a temporal striped pattern ornament to woo male partners [5] These examples demonstrate that complex eukaryotic organisms can employ visual, vocal, or mechanical tactics to secure a mate and transmit their genetic traits to the generation. An ascomycete, undergoes a white-opaque switch to initiate mating [8] Despite their divergent sexual strategies, these morphological transitions are all controlled by the pheromone response pathway [9]. These studies establish that the pheromone response pathway plays a critical role in promoting fungal mating efficiency
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