American Society of Naturalists

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“Mating system evolution under strong pollen limitation: Evidence of disruptive selection through male and female fitness in Clarkia xantiana”

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Ryan D. Briscoe Runquist, Monica A. Geber, Michael Pickett-Leonard, and David A. Moeller

Divergent selection via male and female fitness of floral traits and the evolution of intermediate outcrossing rates

Sexual conflict resolution in plants: the evolution of different mating strategies

Native oligolectic bee visiting the highly outcrossing subspecies of <i>Clarkia xantiana</i>, <i>C.&nbsp;x.&nbsp;xantiana</i>.<br />(Credit: David Moeller)
Native oligolectic bee visiting the highly outcrossing subspecies of Clarkia xantiana, C. x. xantiana.
(Credit: David Moeller)

Plants have enormous variation in their sexuality. Most plant species have flowers that function as both males and females (hermaphroditism). Because most plants are hermaphrodites, they have the potential to mate with themselves (selfing) in addition to mating with other individuals via pollinators (outcrossing). Selfing can be particularly beneficial when plants grow in environments where pollinators are uncommon and reproduction often fails. When populations chronically lack sufficient pollinator service, special floral mechanisms can evolve that facilitate selfing, and this has occurred repeatedly in nature. What remains poorly understood is how natural selection causes the evolution of higher selfing rates and how selection acts through the male versus female function of flowers.

Highly selfing subspecies of <i>Clarkia xantiana</i>,  <i>C.&nbsp;x.&nbsp;parviflora</i>. <br />(Credit: David Moeller)
Highly selfing subspecies of Clarkia xantiana, C. x. parviflora.
(Credit: David Moeller)

To examine this conundrum, Briscoe Runquist, Moeller, and colleagues studied Clarkia xantiana, a California wildflower that contains two closely related subspecies that strongly differ in how much they outcross vs. self-fertilize. The authors created an experimental population that included the two extremes found in nature along with intermediate forms generated by crosses between them. They exposed this highly variable population to field conditions where pollinators were uncommon to see how the range of flowers achieved fitness as males versus females, and which forms were favored by natural selection. The authors also used molecular genetics and paternity analysis to determine which plants were the fathers of the seeds produced by the population.

Highly outcrossing subspecies of <i>Clarkia xantiana</i>,  <i>C.&nbsp;x.&nbsp;xantiana</i>.<br />(Credit: David Moeller)
Highly outcrossing subspecies of Clarkia xantiana, C. x. xantiana.
(Credit: David Moeller)

Contrary to previous findings, the authors found that natural selection favored the two extremes of the range of mating system variation: those plants that were most highly outcrossing and those most highly selfing. Selection disfavored intermediates between them, particularly because they had poor reproductive success as males. These results highlight that variation in male fitness, which is less commonly quantified, can be critical for understanding how plant sexual systems evolve. Moreover, they help explain why divergent, alternative mating strategies are often maintained in nature. Read the Article