Dataset Information

Nectary size is a pollination syndrome trait in Penstemon.

ABSTRACT: Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird-adapted flowers have evolved a remarkable number of times from bee-adapted ancestors in Penstemon, and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative importance of nectar volume and nectary development in defining Penstemon pollination syndromes. We tested the evolutionary association of nectar volume and nectary area with pollination syndrome across 19 Penstemon species. In selected species, we assessed cellular-level processes shaping nectary size. Within a segregating population from an intersyndrome cross, we assessed trait correlations between nectar volume, nectary area, and the size of stamens on which nectaries develop. Nectar volume and nectary area displayed an evolutionary association with pollination syndrome. These traits were correlated within a genetic cross, suggesting a mechanistic link. Nectary area evolution involves parallel processes of cell expansion and proliferation. Our results demonstrate that changes to nectary patterning are an important contributor to pollination syndrome diversity and provide further evidence that repeated origins of hummingbird adaptation involve parallel developmental processes in Penstemon.

SUBMITTER: Katzer AM

PROVIDER: S-EPMC6593460 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Nectary size is a pollination syndrome trait in Penstemon.

Katzer Amanda M AM Wessinger Carolyn A CA Hileman Lena C LC

The New phytologist 20190326 1

Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird-adapted flowers have evolved a remarkable number of times from bee-adapted ancestors in Penstemon, and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative i ...[more]

PMID: 30834532

Similar Datasets

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:A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.

Project description:In many plant species, pollination syndromes predict the most effective pollinator. However, other floral visitors may also offer effective pollination services and promote mixed pollination systems. Several species of the species-rich Penstemon (Plantaginaceae) exhibit a suite of floral traits that suggest adaptation for pollination by both hymenopterans and hummingbirds. Transitions from the ancestral hymenopteran pollination syndrome to more derived hummingbird pollination syndrome may be promoted if the quantity or quality of visits by hummingbirds is increased and if the ancestral pollinator group performs less efficiently. The quantification of such shifts in pollination systems in the group is still limited. We aimed to investigate floral traits linked to this pollination syndrome in Penstemon gentianoides with flowers visited by bumblebees and hummingbirds.We investigated the floral biology, pollinator assemblages, breeding system and nectar production patterns of P. gentianoides inhabiting a temperate montane forest in central Mexico. Pollination experiments were also conducted to assess the pollinator effectiveness of bumblebees and hummingbirds.P. gentianoides flowers are protandrous, with 8-d male phase (staminate) flowers, followed by the ∼1-7 d female phase (pistillate phase). Flowers display traits associated with hymenopteran pollination, including purple flowers abruptly ampliate-ventricose to a broad throat with anthers and stigmas included, and long lifespans. However, the nectar available in the morning hours was abundant and dilute, traits linked to flowers with a hummingbird pollination syndrome. Two hummingbird species made most of the visits to flowers, Selasphorus platycercus (30.3% of all visits), followed by Archilochus colubris (11.3%). Bumblebees (Bombus ephippiatus, B. huntii and B. weisi) accounted for 51.8% of all recorded visits, but their foraging activity was restricted to the warmer hours. Hummingbirds made more foraging bouts and visited more flowers than hymenopteran species. Flowers experimentally pollinated by B. ephippiatus produced significantly more fruits than those pollinated by S. platycercus. However, there was no statistical difference in the number of seeds produced per fruit when a bumblebee or a hummingbird was the pollinator.We have shown that bumblebees and hummingbirds visit and pollinate P. gentianoides flowers. Despite floral traits resembling the hymenoptera pollination syndrome, flowers of P. gentianoides offer characteristic nectar rewards to flowers with a hummingbird pollination syndrome. Although pollination efficiency is higher among flowers visited by hymenoptera, the noteworthy percentage of fruit production and number of seeds per fruit derived from hummingbird pollination highlights the importance of hummingbirds as a functional group of pollinators that might have potential evolutionary consequences to the plants.

Project description:We report genomic traits that have been associated with the life history of prokaryotes and highlight conflicting findings concerning earlier observed trait correlations and tradeoffs. In order to address possible explanations for these contradictions we examined trait-trait variations of 11 genomic traits from ~18,000 sequenced genomes. The studied trait-trait variations suggested: (i) the predominance of two resistance and resilience-related orthogonal axes and (ii) at least in free living species with large effective population sizes whose evolution is little affected by genetic drift an overlap between a resilience axis and an oligotrophic-copiotrophic axis. These findings imply that resistance associated traits of prokaryotes are globally decoupled from resilience related traits and in the case of free-living communities also from traits associated with resource availability. However, further inspection of pairwise scatterplots showed that resistance and resilience traits tended to be positively related for genomes up to roughly five million base pairs and negatively for larger genomes. Genome size distributions differ across habitats and our findings therefore point to habitat dependent tradeoffs between resistance and resilience. This in turn may preclude a globally consistent assignment of prokaryote genomic traits to the competitor - stress-tolerator - ruderal (CSR) schema that sorts species depending on their location along disturbance and productivity gradients into three ecological strategies and may serve as an explanation for conflicting findings from earlier studies. All reviewed genomic traits featured significant phylogenetic signals and we propose that our trait table can be applied to extrapolate genomic traits from taxonomic marker genes. This will enable to empirically evaluate the assembly of these genomic traits in prokaryotic communities from different habitats and under different productivity and disturbance scenarios as predicted via the resistance-resilience framework formulated here.

Project description:Nectaries are a promising frontier for plant evo-devo research, and are particularly fascinating given their diversity in form, position, and secretion methods across angiosperms. Emerging model systems permit investigations of the molecular basis for nectary development and nectar secretion across a range of taxa, which addresses fundamental questions about underlying parallelisms and convergence. Herein, we explore nectary development and nectar secretion in the emerging model taxa, Cleome violacea (Cleomaceae), which exhibits a prominent adaxial nectary. First, we characterized nectary anatomy and quantified nectar secretion to establish a foundation for quantitative and functional gene experiments. Next, we leveraged RNA-seq to establish gene expression profiles of nectaries across three key stages of development: pre-anthesis, anthesis, and post-fertilization. We then performed functional studies on five genes that were putatively involved in nectary and nectar formation: CvCRABSCLAW (CvCRC), CvAGAMOUS (CvAG), CvSHATTERPROOF (CvSHP), CvSWEET9, and a highly expressed but uncharacterized transcript. These experiments revealed a high degree of functional convergence to homologues from other core Eudicots, especially Arabidopsis. CvCRC, redundantly with CvAG and CvSHP, are required for nectary initiation. Concordantly, CvSWEET9 is essential for nectar formation and secretion, which indicates that the process is eccrine based in C. violacea. While demonstration of conservation is informative to our understanding of nectary evolution, questions remain. For example, it is unknown which genes are downstream of the developmental initiators CvCRC, CvAG, and CvSHP, or what role the TCP gene family plays in nectary initiation in this family. Further to this, we have initiated a characterization of associations between nectaries, yeast, and bacteria, but more research is required beyond establishing their presence. Cleome violacea is an excellent model for continued research into nectary development because of its conspicuous nectaries, short generation time, and close taxonomic distance to Arabidopsis.

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.

Dataset Information

Nectary size is a pollination syndrome trait in Penstemon.

Publications

Nectary size is a pollination syndrome trait in Penstemon.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets