To mate, or not to mate: Yeast established as a model of sexual behaviour
It has long been known that animals alter their sexual behaviour depending on the availability of mates. Scientists at the Max Planck Institute for Terrestrial Microbiology have now shown that a sexual unicellular eukaryote, the backer's yeast Saccharomyces cerevisiae, can effectively perceive the ratio of sexes in a mating population. Such sensing of the sex ratio allows yeast to predictively control the investment employed in the sexual response, thus balancing the costs and benefits of sex. The work establishes the yeast mating system as an experimental model to test theories on the evolution of sexual behaviour.
Sexual behaviour in animals depends on the relative abundance of each sex, a quantity known as the operational sex ratio. As first noticed already by Charles Darwin, males have evolved secondary sexual characters that allow them to directly or indirectly compete with other males for the access to females in what is known as intrasexual selection. However, the ways in which animals are able to perceive this sex ratio and respond to it have remained elusive, largely because such perception relies on a number of different chemosensory and visual cues and further evolves complex neural information processing.
Mating of the two sexual forms of Saccharomyces cerevisiae cells, MATa and MATα, involves mutual chemosensory communication based on peptide pheromones, where MATa cells secrete a-factor and MATα cells secrete α-factor. Each mating type responds to the pheromone produced by the other mate via a signal transduction pathway that activates expression of mating genes and induces mating-specific changes in morphology. Additionally, MATa cells produce an extracellular protein Bar1 that degrades the α-factor (that is, mating signal emitted by the opposite sex) – at the first sight a "paradoxical" activity.
Previous studies of yeast mating have almost invariantly considered a scenario where mating occurred between individual cell immobilized on a solid surface. In this scenario, the main function of sexual pheromones is to inform yeast about the direction towards the closest mating partner, stimulating formation of a mating projection into this direction. However, because yeast cannot move, such mating on a surface requires cells of different mating type to be in an immediate proximity to each other.
Marburg scientists decided to challenge this established view. “While surface mating is a convenient depiction of the laboratory conditions, in the real world yeast cells rarely come into direct contact” says Prof. Victor Sourjik. “A much more realistic scenario would be mating in a stirred suspension, be it a drop of rainwater or an insect gut, where yeast cells need to first randomly collide with a mating partner and then specifically attach to it before initiating mating. We realized that in yeast efficiency of sexual aggregation rather than the ability to sense pheromone gradients might be the main determinant of sexual behaviour”.
What information could then be provided by pheromones in this new scenario of mating in suspension? An obvious answer to this question was that pheromone concentrations reflect abundance of the two mating types in the population. "We basically shifted the view of yeast pheromone signalling from a distance-cue to an abundance-cue scenario” says Dr. Alvaro Banderas, a postdoctoral fellow in Sourjik’s lab. “By reflecting abundance of its mating partners, the pheromone signal also informs the yeast how likely it is to find a mate. Moreover, the “paradoxical” function of Bar1 also became clear – it allows yeast to measure the degree of sexual competition, by degrading the pheromone secreted by the mating partner dependent on the density of same-sex individuals. Thus, each cell would then not only respond to the abundance of potential partners, but would also attenuate the response according to the number of competitors.”
Yeast apparently indeed uses this information about availability of mates and competitors to tune its investment into mating, including expressing of sexual agglutinins that enhance aggregation. A combination of experimental analysis with mathematical modelling showed that this strategy allows a precise and optimal matching of the investment to the actual mating probability. “While mating might be advantageous, it is also highly costly, and thus investing resources only when you are likely to find a mate represents an optimal strategy for yeast sexual behaviour” says Prof. Victor Sourjik. “This provides really interesting parallels to sexual behaviour in animals. It shows that one does not need complex neural system to exhibit the anticipatory sexual behaviour – simple unicellular eukaryotes can do it, too.”
Banderas A, Koltai M, Anders A, Sourjik V (2016) Sensory input attenuation allows predictive sexual response in yeast. Nat Commun 7:12590. doi: 10.1038/ncomms12590.