A major transition in evolution is the shift from asexual to sexual reproduction in early organisms. But why would a yeast cell, which usually reproduces asexually, choose to mate with a very different partner in times of stress?
Timelapse following the mating of a fission yeast gamete pair. The blue marker is expressed in one gamete and spreads as both gametes fuse. Magenta marks the nuclei fusing and dividing. Green marks a meiotic factor, which is induced in one gamete first and then degraded during meiosis. Credit: Vjestica lab, Center for Integrative Genomics, University of Lausanne, Switzerland.
Differences between two sex cells, like a sperm and egg, are known as sexual asymmetry.
This property first evolved in single-cell organisms, which usually reproduce asexually (one cell splitting to become two genetically identical cells) but can transition to reproduce sexually (two separate cells called gametes fusing to produce a genetically unique cell) during periods of stress. This is when genetic variation can help the species become better adapted to a changing environment.
Zena Hadjivasiliou, group leader of the Mathematical and Physical Laboratory at the Crick, first became interested in sexual asymmetry during her PhD, when she used theoretical modelling to understand why the emergence of two mating types would be evolutionarily beneficial.
In a new research study published today in PNAS, Zena’s lab at the Crick joined forces with Aleksandar Vještica’s team at the University of Lausanne, to investigate why, during sexual reproduction, the two mating yeast cells (or gametes) look exactly the same but are split into two different mating types and distinct roles during mating.
“It’s easy to understand the differences in the roles of sex cells when they also look very different, like a sperm and egg,” says Zena. “The egg provides most of the nutritional content for the offspring whereas the sperm are good swimmers and can carry new genetic material from afar. But when two cells look exactly the same, as we see in yeast, the need for different roles isn’t as clear.”
The international team found that the two yeast mating types, known as P and M, produce different amounts of proteins needed for a key stage of sexual reproduction called meiosis. Aleksander’s team looked at yeast cells in the lab, finding that the proteins, called meiotic factors, are essential for meiosis and need to be produced before P and M gametes fuse to become a single cell.
But they also found an interesting trade-off between sexual and asexual reproductive success. If fusion failed, the yeast cells with large amounts of meiotic factors struggled to then divide asexually, where one cell simply splits in two.
“My initial observation of parental asymmetry in meiotic protein production was so unexpected that I immediately called my team to the microscopy room to share my surprise,” says Celso Martins, a postdoctoral researcher at the University of Lausanne who carried out the experimental work. “I was then stunned again by the biological consequences of this molecular asymmetry: the partner that supplies more of the meiotic factors does so at risk of dying if it fails to fuse with a partner.”
To further understand the evolutionary trade-off, Harry Booth, a senior laboratory research scientist in Zena’s team who carried out the theoretical work, developed a computational model to complement the experimental studies. He simulated the life cycles of the yeast cells, and combined this with mathematical modelling, to show that there was a critical threshold of total meiotic factor investment needed for meiosis, above which a requirement for an asymmetric contribution from the two mating types would appear.
Armed with this prediction, the Lausanne team genetically changed yeast cells to produce different amounts of the meiotic factors, and then measured how well the individual cells (gametes) and the fused cell (the zygote, or offspring) survived. Their results matched the prediction of Harry’s simulations: when the team increased the amount of these factors, they found that the fused cell, the offspring, was more likely to survive. But at the same time, individual gametes carrying high levels of these factors were less able to survive on their own.
“This showed that yeast need a lot of meiotic factors for sexual reproduction to work, but they’re actually detrimental for the survival of the individual gametes,” Harry explains. “Splitting the factors 50-50 would mean both cells are likely to die if meiosis fails, whereas splitting them unequally between two different mating types ensures at least one cell would survive if meiosis doesn’t work.”
The team thinks that, over time, these simple differences may have laid the groundwork for the evolution of the more familiar physical distinctions we see in sex cells like sperm and egg today.
“What’s interesting is that this isn’t about making each individual cell more successful, it’s about ensuring that at least one path leads to a viable offspring,” concludes Zena. “Different mating types and the very first asymmetries between fusing gametes may have evolved as a way to deal with opposing pressures at different stages of a species life cycle.”
Reflecting on the work, Aleksandar says, “What was most striking to us is that fission yeast gametes look completely identical, yet they clearly make distinct contributions to their offspring. Fission yeast lets us see how partner gamete asymmetries arise at the molecular level, in a system simple enough to manipulate directly to test our ideas — something that's nearly impossible to do in species where the sexes are already visibly different.”
