“The effect of pollen limitation on the evolution of mating system and seed size in hermaphroditic plants”

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Qiaoqiao Huang and Martin Burd (Mar 2019)

The DOI will be https://dx.doi.org/10.1086/701782

This study identifies a novel pathway through which pollen limitation selects for reproductive assurance and mixed mating, and provides an adaptive explanation as to why selfed seeds are often smaller than outcrossed seeds

Pollen limitation of plant reproduction is becoming increasingly common in nature because of factors such as human disturbance, habitat loss or fragmentation, and climate change, which may reduce plant and pollinator abundance. Pollen limitation may increase the optimal seed size in outcrossing plants. Pollen limitation may also promote the evolution of self-fertilization as a mechanism of reproductive assurance. Previous models of self-fertilization assume a constant seed size, and most of them predict that either complete outcrossing or complete selfing should evolve. However, the effect of pollen limitation on the joint evolution of mating system and seed size is not known.

Here, Huang and Burd model how mating system and seed size jointly evolve in hermaphroditic plants under pollen limitation. Pollen limitation in their study means that the fraction of ovules fertilized by outcrossed pollen is less than one. However, the fraction of selfed ovules fertilized is always one, meaning that selfed ovules are never pollen limited, which is likely true for autogamy with prior or delayed mode of self-fertilization. The authors also consider two contrasting assumptions about the fraction of ovules fertilized. In the first, this fraction is independent of ovule production, meaning that the number of ovules fertilized by outcrossed pollen increases linearly with ovule production. In the second, this fraction decreases with ovule production, meaning that the number of ovules fertilized by outcrossed pollen increases less rapidly than ovule production.

When the fraction of ovules fertilized is independent of ovule production, Huang and Burd find that either complete outcrossing or complete selfing should evolve. When the fraction of ovules fertilized decreases with ovule production, mixed mating may evolve. This is because the marginal fitness returns from resource investment in the production of outcrossing ovules decrease with ovule production, but those from investment in the production of selfed seeds are a constant value. Therefore, as ovules produced for outcrossing reach a certain number, resource investment in outcrossing reproduction and selfed seeds should obtain the same marginal fitness returns, and plants should allocate the remaining resources to the production of selfed seeds. Under mixed mating, to meet the requirement that the marginal fitness returns through resource investment are equal for an outcrossed seed and a selfed seed, outcrossed seeds should be larger than selfed seeds.

The model therefore identifies a novel pathway through which pollen limitation selects for reproductive assurance and mixed mating, and provides an adaptive explanation as to why selfed seeds are often smaller than outcrossed seeds.


Abstract

Pollen limitation, when inadequate pollen receipt results in a plant setting fewer seeds and fruits, can reduce plant reproductive success and promote the evolution of self-fertilization as a mechanism of reproductive assurance. However, the effect of pollen limitation on the joint evolution of mating system and seed size is not known. Using an evolutionarily stable strategy (ESS) resource allocation model, we show that where moderate pollen limitation and strong inbreeding depression select for complete outcrossing, pollen limitation should also increase the optimal seed size. In contrast, pollen limitation should not affect the optimal seed size under complete selfing, in which case ovule fertilization is certain. Under intermediate conditions, a mixed mating system evolves if the probability of ovule fertilization declines as more ovules are produced, so that a selfed seed with inbreeding depression provides equal marginal fitness returns to a larger outcrossed seed that may result from pollen limitation. Under mixed mating, outcrossed seeds should be larger than selfed seeds, and pollen limitation should not affect the optimal size of either outcrossed or selfed seeds. Our results identify a novel pathway through which pollen limitation selects for mixed mating, and provide an adaptive explanation as to why selfed seeds are often smaller than outcrossed seeds.