Dataset Information

Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants.

ABSTRACT:

Background and aims

Most theory addressing the evolution of pollen limitation in flowering plants focuses on stochasticity in the relative abundance of plant and pollinator populations affecting trade-offs in resource allocation to ovule production or pollinator attraction vs. seed maturation. Mating system evolution is an underappreciated but potentially widespread additional mechanism for the evolutionary emergence of pollen limitation in animal-pollinated self-compatible plants.

Methods

We model individual plant flowering phenologies influencing both pollinator attraction and geitonogamous self-fertilization caused by pollinator movements among flowers within plants, incorporating demographic but not environmental stochasticity. Plant phenology and the resulting pollen limitation are analysed at evolutionarily stable equilibria (ESS). Pollen limitation is measured by two quantities: the proportion of unpollinated flowers and the reduction in maternal fitness caused by inbreeding depression in selfed seeds.

Key results

When pollinators visit multiple flowers per plant, pollen limitation is never minimized at an ESS and results from the evolution of flowering phenologies balancing the amount and genetic composition (outbred vs. inbred) of pollen receipt.

Conclusions

Results are consistent with previous theory demonstrating that pollen limitation can be an evolved property, not just a constraint; they complement existing models by showing that plant avoidance of inbreeding depression constitutes a genetic mechanism contributing to evolution of pollen limitation, in addition to ecological mechanisms previously studied.

SUBMITTER: Devaux C

PROVIDER: S-EPMC6344218 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Publications

Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants.

Devaux Céline C Porcher Emmanuelle E Lande Russell R

Annals of botany 20190101 2

<h4>Background and aims</h4>Most theory addressing the evolution of pollen limitation in flowering plants focuses on stochasticity in the relative abundance of plant and pollinator populations affecting trade-offs in resource allocation to ovule production or pollinator attraction vs. seed maturation. Mating system evolution is an underappreciated but potentially widespread additional mechanism for the evolutionary emergence of pollen limitation in animal-pollinated self-compatible plants.<h4>Me ...[more]

PMID: 30351386

Similar Datasets

Project description:Background and aimsVariation in inbreeding depression (?) among individual plants is considered to play a central role in mating system evolution and population genetics. Moreover, such variation could be linked to individual susceptibility to pollen limitation (PL) because those individuals strongly affected by ? for seed production will require more outcross pollen for setting a given number of fruits or seeds. However, no study has tested explicitly for associations between PL and ? at the individual plant level. This study assesses the extent of among-individual variation in PL and ?, the consistency of ? across life stages, and the relationships between individual PL and ? in the mixed-mating shrub Myrtus communis.MethodsControlled hand-pollinations were performed in a natural M. communis population. Marked flowers were monitored until fruit production and a greenhouse experiment was conducted with the seeds produced.Key resultsCompared with selfing, outcross-pollination enhanced seed number per fruit, germination rate and seedling growth, but did not enhance fruit-set. Only seed number per fruit was pollen limited and, thus, cumulative pollen limitation depended more on pollen quality (outcross pollen) than on quantity. The effects of ? varied considerably across life stages and individual plants. Cumulative ? was high across individuals (mean ? = 0·65), although there were no positive correlations between ? values at different life stages. Interestingly, maternal plants showing stronger ? for seed production were more pollen limited, but they were also less affected by ? for seedling growth because of a seed size/number trade-off.ConclusionsResults show a general inconsistency in ? across life stages and individuals, suggesting that different deleterious loci are acting at different stages. The association between ? and PL at the individual level corroborates the idea that pollen limitation may be 'genotype-dependent' regardless of other factors.

Project description:Background and aimsAlthough pollen limitation of reproduction (PL) has been widely studied, our understanding of its occurrence in tropical communities, especially for bird-pollinated plants, is underdeveloped. In addition, inclusion of both quantity and quality aspects in studies of PL are generally lacking. Within hummingbird-pollinated plants, a prediction was made for higher PL for the quality than quantity aspects and a minor effect of temporal variation because hummingbirds are constant and efficient pollen vectors but they may transfer low quality pollen.MethodsField hand and open pollination experiments were conducted on 21 species in a tropical montane rain forest over 2 years. The quantity (fruit set and seeds per fruit) and quality (seed weight and germination) aspects of reproduction were assessed as the response to open pollination relative to outcross hand pollination. The relationships between the effect size of quantity and quality aspects of reproduction and predictive plant features (self-incompatibility, autogamy, density and pollinator specialization level) were assessed with phylogenetic generalized linear models.Key resultsJust over half of all the species expressed PL for one or more response variables. On average, the severity of PL was strong for one quality variable (seed germination; 0·83), but insignificant for another (seed weight; -0·03), and low to moderate for quantity variables (0·31 for seeds per fruit and 0·39 for fruit set). There was only a minor contribution of temporal variation to PL within the studied species. Common predictors of PL, i.e. phylogenetic relatedness, self-incompatibility, autogamy, plant density and pollinator specialization level, did not adequately explain variation in PL within this community.ConclusionsDespite the measurable degree of PL within these hummingbird-pollinated plants, the causes of pollen quality and quantity insufficiency are not clear. Variables other than those tested may contribute to PL or causes of PL may vary among species and cannot adequately be accounted for when assessed from the within-community perspective.

Project description:Avoiding inbreeding, and therefore avoiding inbreeding depression in offspring fitness, is widely assumed to be adaptive in systems with biparental reproduction. However, inbreeding can also confer an inclusive fitness benefit stemming from increased relatedness between parents and inbred offspring. Whether or not inbreeding or avoiding inbreeding is adaptive therefore depends on a balance between inbreeding depression and increased parent-offspring relatedness. Existing models of biparental inbreeding predict threshold values of inbreeding depression above which males and females should avoid inbreeding, and predict sexual conflict over inbreeding because these thresholds diverge. However, these models implicitly assume that if a focal individual avoids inbreeding, then both it and its rejected relative will subsequently outbreed. We show that relaxing this assumption of reciprocal outbreeding, and the assumption that focal individuals are themselves outbred, can substantially alter the predicted thresholds for inbreeding avoidance for focal males. Specifically, the magnitude of inbreeding depression below which inbreeding increases a focal male's inclusive fitness increases with increasing depression in the offspring of a focal female and her alternative mate, and it decreases with increasing relatedness between a focal male and a focal female's alternative mate, thereby altering the predicted zone of sexual conflict. Furthermore, a focal male's inclusive fitness gain from avoiding inbreeding is reduced by indirect opportunity costs if his rejected relative breeds with another relative of his. By demonstrating that variation in relatedness and inbreeding can affect intra- and inter-sexual conflict over inbreeding, our models lead to novel predictions for family dynamics. Specifically, parent-offspring conflict over inbreeding might depend on the alternative mates of rejected relatives, and male-male competition over inbreeding might lead to mixed inbreeding strategies. Making testable quantitative predictions regarding inbreeding strategies occurring in nature will therefore require new models that explicitly capture variation in relatedness and inbreeding among interacting population members.

Dataset Information

Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants.

Background and aims

Methods

Key results

Conclusions

Publications

Mating systems and avoidance of inbreeding depression as evolutionary drivers of pollen limitation in animal-pollinated self-compatible plants.

Similar Datasets

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