Flowers evolve to balance the risks and rewards of self-pollination

The longer a plant waits to self-pollinate, the longer it has to attract pollen from outside. But waiting too long can have consequences.

Laura Hildesheim and colleagues found Dalechampia scandens changes the herkogamy, the internal arrangement of its flowers that separates male and female organs when pollinators are scarce to aid self-pollination. “This suggests that, in the context of declining pollinator populations, evolutionary shifts toward greater rates of autonomous self-pollination can be rapid,” conclude the authors.

The varying arrangements of sexual organs in D. scandens over time. Full details in Hildesheim et al. (2019).

Herkogamy, the separation of the male and female organs in space, and dichogamy, the separation in time, evolved to reduce the chance of self-pollination. If the organs ripen at different times and are not close, then pollen is more likely to arrive from another plant. However, if pollinators are limited, then the ovule is left waiting for pollen that never comes. In this case, self-pollination is better than no seed set at all, but this wait has consequences. The longer a plant waits to self-pollinate, the poorer quality its own pollen will be. Hildesheim and colleagues investigated how plants react to the changing availability of pollinators, and if this affected self-pollination.

The team conducted three experiments. They examined how herkogamy and dichogamy varied in populations of D. scandens in a greenhouse, and how these same traits varied in the wild, with differing pollinator availability. Finally, they tested how delays in selfing affected seed quality and quantity.

They found that herkogamy varied with pollinator availability, but dichogamy did not. “This is consistent with the results of an earlier study finding an association of pollinator abundance with herkogamy but not protandry in Clarkia xantiana,” wrote the authors, “even though both traits affect reproductive success via autonomous selfing, and thus should be selected similarly by the pollination environment…”

The botanists also found that reproductive performance was best in the flowers early in their life. “When late pollination yielded seeds, these were fewer and smaller than those obtained by early pollination. In D. scandens, reduced seed production by old flowers often occurred through complete seed set failure of individual flowers within a blossom, while the other flowers produced near-maximum seed set…,” say the authors. This decline would confirm that there are consequences for waiting too long to self-pollinate.

The penalities for self-pollination mean that, so long as there are pollinators about, there is a strong preference for cross-pollination. The delayed-selfing of flowers would help depress the success of self-pollinating flowers compared to the plants that could attract pollinators. However, if pollinators fail, then circumstances change. “This process would not preclude the evolution towards earlier selfing under complete pollination failure but could contribute to the maintenance of a stable mixed mating system via the maintenance of protogyny,” say the authors. “Furthermore, it could constrain the evolution towards competing selfing or complete autonomous selfing as long as some cross-pollination occurs.”

These results do leave open a question of why herkogamy is so flexible, when dichogamy isn’t. However, it is possible that dichogamy still leaves a window for cross-pollinating plants to outcompete selfing plants. For D. scandens, success in pollination may be a matter of timing.