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On the function of flower number: disentangling fertility from pollinator-mediated selection.

ABSTRACT: In animal-pollinated angiosperms, the 'male-function' hypothesis claims that male reproductive success (RS) should benefit from large floral displays, through pollinator attraction, while female RS is expected to be mainly limited by resource availability. As appealing as this theory might be, studies comparing selection strength on flower number in both sexes rarely document the expected asymmetry. This discrepancy could arise because flower number impacts both pollinator attraction and overall gamete number. In this study, we artificially manipulate floral displays to disentangle the fertility versus pollinator attraction components of selection, both in terms of mating and RS. In females, flower number was under strong fertility selection, as predicted in the absence of pollen limitation. By contrast, in males, flower number was mainly under sexual selection, which in turn increased male RS. However, these selection patterns were not different in males with artificially increased floral displays. This suggests that sexual selection acting on flower number in males does not occur because flower number increases pollinator attraction, but rather because more pollen is available to disperse on more mates. Our study illustrates the power of disentangling various components of selection with potentially sex-specific effects for understanding the evolution of sexual dimorphism.

SUBMITTER: Barbot E

PROVIDER: S-EPMC9709571 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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On the function of flower number: disentangling fertility from pollinator-mediated selection.

Barbot Estelle E Dufaÿ Mathilde M Tonnabel Jeanne J Godé Cécile C De Cauwer Isabelle I

Proceedings. Biological sciences 20221130 1987

In animal-pollinated angiosperms, the 'male-function' hypothesis claims that male reproductive success (RS) should benefit from large floral displays, through pollinator attraction, while female RS is expected to be mainly limited by resource availability. As appealing as this theory might be, studies comparing selection strength on flower number in both sexes rarely document the expected asymmetry. This discrepancy could arise because flower number impacts both pollinator attraction and overall ...[more]

PMID: 36448279

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Project description:Background and aimsIn animal-pollinated plants, direct and indirect selection for large and small flowers in predominantly outcrossing and selfing species, respectively, is a common consequence of pollen limitation (PL). However, many hermaphroditic species show a mixed-mating system known as delayed selfing, which provides reproductive assurance (RA) only when outcrossing is not realized. Although RA is expected to reduce pollinator-mediated selection towards larger flowers, the consequences of delayed selfing for selection on flower size in mixed-mating species remain overlooked. We investigated whether RA weakens selection on flower size in Tuberaria guttata, a mixed-mating annual herb.MethodsWe related pollinator visitation rates to flower size and measured seed production in emasculated, hand cross-pollinated and intact (control) flowers in three natural populations. For each population, we estimated variation in PL and RA across individuals differing in flower size and phenotypic selection on this trait.Key resultsPollinator visitation increased and RA decreased with flower size in all populations. Increasing RA diminished but did not fully alleviate PL, because of early-acting inbreeding depression. In the least-visited and most pollen-limited population, RA increased seed production by >200 %, intensely counteracting the strong pollinator-mediated selection for larger corollas. In the most-visited population, however, RA increased seed production by an average of only 9 %. This population exhibited the largest fraction of individuals that showed a decrease in seed production due to selfing and the weakest pollinator-mediated selection on flower size.ConclusionsThe results suggest that the balance between the extent of RA and outcrossing contributes to determine flower size in mixed-mating systems. Pollinator-mediated selection favours larger flowers by increasing outcrossed seeds, but the benefits of RA greatly lessen this effect, especially under severe conditions of pollen limitation. Our findings also indicate that a mixed-mating system can represent an 'evolutionary trap' under an adequate pollinator supply.

Project description:Background and aimsSelection exerted by pollinators on flowers is predicted to occur along two distinct axes. While pollinator attraction to flowers is governed by pollinator preferences, pollen transfer efficiency is mediated by the mechanical fit of pollinators to flower morphology. Although pollinator attraction in sexually deceptive orchids is typically underpinned by floral odour, morphological traits are expected to play a vital role in mechanical fit during floral contact with pollinators.MethodsHere we utilize a comprehensive and novel procedure to test for pollinator-mediated selection through mechanical fit with the flower labellum in the orchid Chiloglottis trapeziformis. This approach combines detailed pollinator observations related to plant reproductive fitness with complementary experimental manipulation and phenotypic selection analysis.Key resultsExperiments with virgin flowers revealed that pollen removal occurs only during vigorous pseudocopulation. This behaviour involves male wasps that grasp the insectiform callus structure on the labellum while probing the labellum tip in a forward orientation. Both orientation and duration of pseudocopulation were significant predictors of pollen removal, confirming a direct relationship between pollinator behaviour and plant fitness. Controlled floral manipulation that either shortened or elongated the distance between the callus and the labellum tip detected no change in pollinator attraction. The duration of pseudocopulation, however, was significantly reduced on flowers with shortened or elongated callus-tip distances, consistent with stabilizing selection. Phenotypic selection analysis confirmed this prediction in natural populations by uncovering evidence for stabilizing selection on the distance between the callus and the labellum tip.ConclusionsOur experimental manipulations and selection analysis in natural populations thus demonstrate stabilizing selection on the distance from the callus to the labellum tip, and illustrate the utility of employing multiple approaches to confirm selection exerted by pollinators on floral form.

Project description:Gentiana leucomelaena manifests dramatic flower color polymorphism, with both blue- and white-flowered individuals (pollinated by flies and bees) both within a population and on an individual plant. Previous studies of this species have shown that pollinator preference and flower temperature change as a function of flower color throughout the flowering season. However, few if any studies have explored the effects of flower color on both pollen viability (mediated by anther temperature) and pollinator preference on reproductive success (seed set) in a population or on individual plants over the course of the entire flowering season. Based on prior observations, we hypothesized that flower color affects both pollen viability (as a function of anther temperature) and pollen deposition (as a function of pollinator preference) to synergistically determine reproductive success during the peak of the flowering season. This hypothesis was tested by field observations and hand pollination experiments in a Tibetan alpine meadow. Generalized linear model and path analyses showed that pollen viability was determined by flower color, flowering season, and anther temperature. Anther temperature correlated positively with pollen viability during the peak of the early flowering season, but negatively affected pollen viability during the peak of the mid- to late flowering season. Pollen deposition was determined by flower color, flowering season (early, or mid- to late season), and pollen viability. Pollen viability and pollen deposition were affected by flower color that in turn affected seed set across the peak of the flowering season (i.e., when the greatest number of flowers were being pollinated). Hand pollination experiments showed that pollen viability and pollen deposition directly influenced seed set. These data collectively indicate that the preference of pollinators for flower color and pollen viability changed during the flowering season in a manner that optimizes successful reproduction in G. leucomelaena. This study is one of a few that have simultaneously considered the effects of both pollen viability and pollen deposition on reproductive success in the same population and on individual plants.

Dataset Information

On the function of flower number: disentangling fertility from pollinator-mediated selection.

Publications

On the function of flower number: disentangling fertility from pollinator-mediated selection.

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