Selection on pollen and pistil traits during pollen competition is affected by both sexual conflict and mixed mating in a self-compatible herb (original) (raw)
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American Journal of Botany, 2007
To increase our knowledge about mating-system evolution, we need to understand the relationship between specific floral traits and mating system. Species of Collinsia (Plantaginaceae) vary extensively in mating system; this variation is associated with variation in floral morphology and development and with the timing of self-pollination. Counterintuitively, large-flowered, more outcrossing species tend to have delayed stigma receptivity, reducing the amount of time that the stigma is receptive to crosspollination before autonomous self-pollination. To understand how the timing of stigma receptivity is related to mating-system evolution, we studied in detail the timing of both stigma receptivity and self-pollination (anther-stigma contact) in two greenhouse-grown populations of large-flowered Collinsia heterophylla. Crosses on emasculated flowers at different stages of floral development always produced seeds, suggesting that cross-fertilization can be effected by pollen arriving prior to physiological receptivity. Phenotypic and genetic variation within populations in the timing of stigma receptivity and antherstigma contact was substantial, although slightly less for the contact. Despite strong interspecific and interpopulation correlations, we did not find an among-genet phenotypic correlation between the traits. This indicates that each trait may respond independently to selection, and the trait association may be the result of correlational selection.
Perspectives in Plant Ecology, Evolution and Systematics, 2010
Studies of sexual selection in plants historically have focused on pollinator attraction, pollen transfer, gametophytic competition, and post-fertilization discrimination by maternal plants. Pollen performance (the speeds of germination and pollen tube growth) in particular is thought to be strongly subject to intrasexual selection, but the effect of mating system on this process has not been rigorously evaluated. Here we propose four predictions derived from the logic that pollen performance should evolve with mating system as an adaptive response to: (1) the competitive environment among pollen genotypes and (2) variation among female genotypes regularly encountered by a given pollen genotype. First, as previously predicted, due to the higher potential for intense selection among diverse pollen genotypes in outcrossing relative to selfing taxa, pollen should evolve to germinate and/or to grow more rapidly in outcrossers than in selfers. Second, due to stronger selection on pollen performance in outcrossing than in selfing taxa, heritable variation in pollen tube growth rate is more likely to be purged in outcrossers. In selfers, by contrast, genetic variation in pollen tube growth rates may readily accumulate because selfing reduces the number of genetically distinct male gametophytes likely to be deposited on any given stigma, thereby relaxing selection on male gametophytic traits. A summary of published studies presented here provides preliminary support for this prediction. Third, due to the high probability that the pollen of outcrossing individuals will be exposed to multiple pistil genotypes, we predict that the pollen of habitually outcrossing taxa will evolve to perform more consistently across female genotypes than the pollen of selfing taxa. Fourth, we predict that epistatic interactions between pollen and pistil genotypes are more likely to evolve in selfers than in outcrossers. We suggest several empirical approaches that may be used to test these predictions.
Interspecific competition in pollination systems: costs to male fitness via pollen misplacement
Functional Ecology, 2012
1. Although competition for pollination is often invoked as a driver of broad-scale evolutionary and ecological patterns, we still lack a clear understanding of the mechanics of such competition. When flower visitors alternate between two species of flower, heterospecific pollen transfer takes place. The impact of these mixed loads on the female reproductive success of a recipient has received considerable attention, but the concomitant loss of male reproductive success -because of pollens grains being lost to foreign stigmas -has received less. Furthermore, pollen losses are not limited to grains that land on stigmas, but can also include deposition on non-stigmatic surfaces of the intervening flowers, or loss from the animal's body through passive detachment or active grooming. We collectively term these losses because of competition 'pollen misplacement'. 2. Here, we quantify pollen transferred by nectar bats between focal flowers (Aphelandra acanthus) with and without intervening visits to one of two competitor species. One competitor (Centropogon nigricans) places its pollen in the same region of bats' heads as the focal species, while the other (Burmeistera sodiroana) places its pollen farther forward. 3. We found that (i) any intervening visit caused some reduction in the number of pollen grains transferred, (ii) competitor flowers with similar pollen-placement locations caused greater reductions in pollen transfer and (iii) of these competitors, those in male phase (dispensing pollen) caused greater pollen loss than those in female phase (without pollen). 4. This study provides rare empirical support for the detrimental effects of competition for pollination on male fitness via pollen misplacement and is the first to show an added cost imposed by male-phase competitors. Although this competition is especially strong when competitors overlap in pollen placement, diverging in pollen placement will not completely eliminate pollen loss during visits to foreign flowers, simply because pollen sheds or is groomed from pollinator's bodies at some background rate over time. This suggests that any angiosperms that share pollinators face pervasive selection through male fitness to diverge in floral traits, alleviating competition by attracting different pollinators, altering floral phenology or encouraging floral constancy.
Plants, 2013
We tested three predictions regarding the joint evolution of pollen performance and mating system. First, due to the potential for intense intrasexual competition in outcrossing populations, we predicted that outcrossers would produce faster-growing pollen than their selfing relatives. Second, if elevated competition promotes stronger selection on traits that improve pollen performance, then, among-plant variation in pollen performance would be lower in outcrossers than in selfers. Third, given successive generations of adaptation to the same maternal genotype in selfers, we predicted that, in selfing populations (but not in outcrossing ones), pollen would perform better following self-than cross-pollinations. We tested these predictions in field populations of two pairs of Clarkia (Onagraceae) sister taxa. Consistent with our predictions, one outcrosser (C. unguiculata) exhibited faster pollen germination and less variation in pollen tube growth rate (PTGR) among pollen donors than its selfing sister species, C. exilis. Contrary to our predictions, the selfing C. xantiana ssp. parviflora exhibited faster PTGR than the outcrossing ssp. xantiana, and these taxa showed similar levels of variation in this trait. Pollen performance following self-vs. cross-pollinations did not differ within either selfing or outcrossing taxa. While these findings suggest that mating system and pollen performance may jointly evolve in Clarkia, other factors clearly contribute to pollen performance in natural populations.
Evolution; international journal of organic evolution, 2018
Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on post-copulatory male traits affecting siring success. In plants, closely related self- and cross-pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse-raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self-pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We t...
DOES POLLEN COMPETITION REDUCE THE COST OF INBREEDING? 1
We hypothesize that floral features promoting pollen competition in angiosperms may have evolved, in some cases, in response to selection generated by the negative effects of inbreeding, at least in plants with mixed-mating systems. Screening of haploid genotypes through pollen competition may purge recessive (or additive) deleterious alleles that are expressed in haploid pollen and hence may reduce the fitness cost of self-pollination, geitonogamy, or biparental inbreeding. We tested one prediction of this hypothesis, that offspring produced by more intense competition among self-pollen have higher fitness than offspring produced by less intense competition. Dalechampia scandens (Euphorbiaceae) flowers were pollinated with pollen from other flowers on the same plant (geitono-gamous self-fertilization). Those flowers experiencing more intense pollen competition as a result of low pollen dispersion (positional variance) on the stigma produced heavier seeds and seedlings with faster-growing radicles than flowers experiencing less intense pollen competition (high pollen dispersion), as predicted by our hypothesis.
The Scope for Postmating Sexual Selection in Plants
Trends in Ecology & Evolution, 2021
Sexual selection is known to shape plant traits that affect access to mates during the pollination phase, but it is less well understood to what extent it affects traits relevant to interactions between pollen and pistils after pollination. This is surprising, because both of the two key modes of sexual selection, male-male competition and female choice, could plausibly operate during pollen-pistil interactions where physical male-female contact occurs. Here, we consider how the key processes of sexual selection might affect traits involved in pollen-pistil interactions, including 'Fisherian runaway' and 'good-genes' models. We review aspects of the molecular and cellular biology of pollen-pistil interactions on which sexual selection could act and point to research that is needed to investigate them.
Correlations among fertility components can maintain mixed mating in plants
American …, 2009
Classical models studying the evolution of self-fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed-plant species are reported to have rates of self-fertili-zation between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self-fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self-fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing-rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.
Variance in pollen carryover in animal-pollinated plants: Implications for mate choice
Journal of Theoretical Biology, 1988
We used analytical and simulation models to explore the effect of variance in pollen carryover on the diversity of donors contributing pollen to recipient flowers. The analytical model illustrated that as carryover rate drops, fewer donors can be sampled by any pollen recipient, and that this reduction in diversity is highly non-linear. Simulations of variable pollen carryover were carried out for two kinds of plant pollinator systems: (a) those in which little pollen on average is removed from a vector during a flower visit, and (b) those in which a large fraction of the available pollen is removed. In both cases, realized carryover is reduced as variance in carryover of pollen from one flower to the next increases. However, the reduction is disproportionately large in case (b). Introducing simulation results in the analytical projection of donor diversity suggests that in the extreme, variance in carryover can reduce the diversity of pollen "seen" by a flower by up to 70%. Thus, insofar as female choice is an adaptive process in flowering plants (and male fitness is enhanced by multiple opportunities for mating), natural selection should favor floral characters that stabilize pollen carryover rates.