A new study reveals that plant populations do not always have to settle on either self-fertilization or cross-fertilization. Using evolutionary computer simulations, researchers found a previously unknown "volatile mixed" state in which self-compatible and self-incompatible plants can coexist for long periods, even as their proportions continually change. The findings offer new insight into how plant reproductive strategies evolve and may respond to environmental pressures such as climate change and declining pollinator populations.
When it comes to reproduction, plants have options. Some can fertilize themselves, while others rely on pollen from genetically different plants. Many populations even contain a mixture of both strategies. But scientists have long debated whether this mixed approach is truly stable or simply a temporary stage on the way from one reproductive strategy to another.
A new study led by Dr. Tamar Friedlander, Dr. Amit Jangid, and Prof. Ohad Noy Feldheim from the Hebrew University of Jerusalem suggests that the answer may be more complicated than previously thought. Researchers identified a previously undescribed state in which plants capable of self-fertilization and plants that require a partner can coexist over long periods, even though the proportions of each group may fluctuate dramatically.
For flowering plants, the choice between self-fertilization and cross-fertilization comes with important trade-offs.
Self-fertilization can be useful when potential mates or pollinators are scarce. A plant does not have to depend on pollen arriving from another individual in order to reproduce. However, repeatedly reproducing with itself can increase the likelihood that harmful genetic mutations will impact its offspring, a phenomenon known as "inbreeding depression."
Many plants avoid this problem through a genetic mechanism called self-incompatibility, which essentially allows a plant to recognize and reject its own pollen. The system promotes reproduction between genetically different individuals and helps maintain diversity within a population. Self-incompatibility is found in around 40% of plant families and occurs in agriculturally important groups that include wild tomatoes, potatoes, apples, pears, citrus fruits and coffee.
But these systems are not foolproof. Various genetic changes can disrupt the self-incompatibility mechanism, allowing some plants to become self-compatible and fertilize themselves. As a result, populations can contain both self-compatible and self-incompatible plants.
The question is what happens next.
Until now, one influential idea has been that such mixed populations are largely transitional. Eventually, one reproductive strategy should take over. Alternatively, it was proposed that mixed populations could exist in fixed and stable proportions. Friedlander and her colleagues used computer simulations of evolving plant populations to test whether these assumptions necessarily hold.
They found three possible outcomes. A population could become entirely self-compatible, entirely self-incompatible, or remain in a mixed state containing both types.
It was the third outcome that surprised the researchers.
Rather than settling into a stable balance, the proportions of self-compatible and self-incompatible plants could rise and fall considerably over time. Yet despite these fluctuations, neither strategy disappeared. The researchers describe this as a "volatile mixed mode," a population that is constantly changing but nonetheless remains mixed over very long periods.
"What surprised us was that instability does not necessarily mean that a population is on its way to one final state," the researchers said. "In our model, self-compatible and self-incompatible plants can coexist for a very long time while their proportions continually change, even in the absence of fluctuations in external conditions. It suggests that what may look like a temporary or unstable situation in nature could actually be a persistent evolutionary state."
The researchers examined two major forces that can influence which reproductive strategy succeeds. One was the genetic cost of self-fertilization, or how severely offspring are affected by inbreeding. The second involved the tolerance of the molecular recognition system plants use to determine which pollen they accept.
By changing these conditions in their simulations, the team was able to map when each of the three reproductive states was likely to emerge.
The study, published in PRX Life, also produced a counterintuitive result concerning pollen shortages.
A shortage of pollen, which can occur when pollinators are scarce or when plants move into new environments, might be expected to favor self-fertilization. After all, a plant that can reproduce by itself has an apparent advantage when external pollen is difficult to find.
However, the researchers' model showed that pollen limitation could actually expand the conditions under which self-incompatibility is maintained. The reasoning behind this is that pollen limitation puts different selection pressures on the evolution of male and female parts of the self-incompatibility system. When these are taken into account, the outcome was more complex than the simple assumption that fewer pollinators should automatically favor self-fertilization.
The findings may also challenge the idea that the evolutionary shift from self-incompatibility to self-fertilization is necessarily a one-way street. Across much of the conditions tested in the model, populations could potentially move in either direction between reproductive strategies. Under certain conditions, a population that had shifted toward self-fertilization could therefore return to a system favoring cross-fertilization.
The researchers stress that the study is theoretical. Mixed populations containing self-compatible and self-incompatible plants have already been observed in nature, but long-term studies tracking how the proportions of the two groups change are still lacking. Such field studies will be necessary to determine whether the long-lasting fluctuating state predicted by the model occurs in real populations.
Understanding these dynamics could become increasingly important as plants face changing environmental conditions. Climate change, shifting habitats and declining pollinator populations may all alter the pressures that determine how plants reproduce.
By showing that reproductive strategies do not always settle neatly into one state or another, the study offers a new way of thinking about how plant populations adapt and persist.
Rather than evolution always pushing a population toward a single reproductive solution, sometimes the lasting solution may be to keep changing.
