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Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome.

ABSTRACT: Angiosperms exhibit staggering diversity in floral form, and evolution of floral morphology is often correlated with changes in pollination syndrome. The showy, bilaterally symmetrical flowers of the model species Antirrhinum majus (Plantaginaceae) are highly specialized for bee pollination. In A. majus, Cycloidea (CYC), Dichotoma (DICH), Radialis (RAD), and Divaricata (DIV) specify the development of floral bilateral symmetry. However, it is unclear to what extent evolution of these genes has resulted in flower morphological divergence among closely related members of Plantaginaceae differing in pollination syndrome. We compared floral symmetry genes from insect-pollinated Digitalis purpurea, which has bilaterally symmetrical flowers, with those from closely related Aragoa abietina and wind-pollinated Plantago major, both of which have radially symmetrical flowers. We demonstrate that Plantago, but not Aragoa, species have lost a dorsally expressed CYC-like gene and downstream targets RAD and DIV. Furthermore, the single P. major CYC-like gene is expressed across all regions of the flower, similar to expression of its ortholog in closely related Veronica serpyllifolia. We propose that changes in the expression of duplicated CYC-like genes led to the evolution of radial flower symmetry in Aragoa/Plantago, and that further disintegration of the symmetry gene pathway resulted in the wind-pollination syndrome of Plantago. This model underscores the potential importance of gene loss in the evolution of ecologically important traits.

SUBMITTER: Preston JC

PROVIDER: S-EPMC3038713 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome.

Preston Jill C JC Martinez Ciera C CC Hileman Lena C LC

Proceedings of the National Academy of Sciences of the United States of America 20110131 6

Angiosperms exhibit staggering diversity in floral form, and evolution of floral morphology is often correlated with changes in pollination syndrome. The showy, bilaterally symmetrical flowers of the model species Antirrhinum majus (Plantaginaceae) are highly specialized for bee pollination. In A. majus, Cycloidea (CYC), Dichotoma (DICH), Radialis (RAD), and Divaricata (DIV) specify the development of floral bilateral symmetry. However, it is unclear to what extent evolution of these genes has r ...[more]

PMID: 21282634

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Project description:Background and aimsHow generalist plants diverge in response to pollinator selection without becoming specialized is still unknown. This study explores this question, focusing on the evolution of the pollination system in the pollination generalist Erysimum mediohispanicum (Brassicaceae).MethodsPollinator assemblages were surveyed from 2001 to 2010 in 48 geo-referenced populations covering the entire geographic distribution of E. mediohispanicum. Bipartite modularity, a complex network tool, was used to find the pollination niche of each population. Evolution of the pollination niches and the correlated evolution of floral traits and pollination niches were explored using within-species comparative analyses.Key resultsDespite being generalists, the E. mediohispanicum populations studied can be classified into five pollination niches. The boundaries between niches were not sharp, the niches differing among them in the relative frequencies of the floral visitor functional groups. The absence of spatial autocorrelation and phylogenetic signal indicates that the niches were distributed in a phylogeographic mosaic. The ancestral E. mediohispanicum populations presumably belonged to the niche defined by a high number of beetle and ant visits. A correlated evolution was found between pollination niches and some floral traits, suggesting the existence of generalist pollination ecotypes.ConclusionsIt is conjectured that the geographic variation in pollination niches has contributed to the observed floral divergence in E. mediohispanicum. The process mediating this floral divergence presumably has been adaptive wandering, but the adaptation to the local pollinator faunas has been not universal. The outcome is a landscape where a few populations locally adapted to their pollination environment (generalist pollination ecotypes) coexist with many populations where this local adaptation has failed and where the plant phenotype is not primarily shaped by pollinators.

Project description:Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes--bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus. In an F2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.

Project description:Background and aimsDipteran insects are known pollinators of many angiosperms, but knowledge on how flies affect floral evolution is relatively scarce. Some plants pollinated by fungus gnats share a unique set of floral characters (dark red display, flat shape and short stamens), which differs from any known pollination syndromes. We tested whether this set of floral characters is a pollination syndrome associated with pollination by fungus gnats, using the genus Euonymus as a model.MethodsThe pollinator and floral colour, morphology and scent profile were investigated for ten Euonymus species and Tripterygium regelii as an outgroup. The flower colour was evaluated using bee and fly colour vision models. The evolutionary association between fungus gnat pollination and each plant character was tested using a phylogenetically independent contrast. The ancestral state reconstruction was performed on flower colour, which is associated with fungus gnat pollination, to infer the evolution of pollination in the genus Euonymus.Key resultsThe red-flowered Euonymus species were pollinated predominantly by fungus gnats, whereas the white-flowered species were pollinated by bees, beetles and brachyceran flies. The colour vision analysis suggested that red and white flowers are perceived as different colours by both bees and flies. The floral scents of the fungus gnat-pollinated species were characterized by acetoin, which made up >90 % of the total scent in three species. Phylogenetically independent contrast showed that the evolution of fungus gnat pollination is associated with acquisition of red flowers, short stamens and acetoin emission.ConclusionsOur results suggest that the observed combination of floral characters is a pollination syndrome associated with the parallel evolution of pollination by fungus gnats. Although the role of the red floral display and acetoin in pollinator attraction remains to be elucidated, our finding underscores the importance of fungus gnats as potential contributors to floral diversification.

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Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome.

Publications

Gradual disintegration of the floral symmetry gene network is implicated in the evolution of a wind-pollination syndrome.

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