Combinations Of Floral Traits Research Articles

Pollination ecotypes and the origin of plant species.

Ecological niche shifts are a key driver of phenotypic divergence and contribute to isolating barriers among lineages. For many groups of organisms, the history of these shifts and associated trait-environment correlations are well-documented at the macroevolutionary level. However, the processes that generate these patterns are initiated below the species level, often by the formation of ecotypes in contrasting environments. Here, I review the evidence in plants for 'pollination ecotypes' as microevolutionary responses to environmental gradients in pollinator availability. Pollinators are critical for population establishment and persistence in most species, thereby forming part of their fundamental niche. Novel floral trait combinations allow species to exploit particular pollination opportunities in local habitats and evolve primarily through sexual selection due to their effects on mating success. I examine selected case studies on the evolution of pollination ecotypes, including self-pollinating forms, and use these to illustrate challenging practical and conceptual issues. These issues include the paucity of reliable natural history data, the problem of implementing and interpreting reciprocal translocation experiments, and establishing criteria for when allopatric ecotypes should be considered species.

Hybrid Mimulus flowers attract a new pollinator.

Hybridization is common in flowering plants and is believed to be an important force driving adaptation and speciation. The flowers of hybrids often exhibit new trait combinations, which, theoretically, could attract new species of pollinators. In this study, we found that the hybrids between a hummingbird-pollinated species Mimulus cardinalis and a self-pollinated species Mimulus parishii attract bumblebees (Bombus impatiens), a pollinator not attracted to either of the progenitor species. This novel attraction is explained by new combinations of floral traits in hybrids, including, most importantly, petal color, in addition to nectar concentration and corolla size. To understand how petal color variation is perceived by bumblebees, we performed reflectance spectroscopy and multispectral imaging to model the flower appearance in bee vision. This analysis showed that color variation would impact the ease of detection. We also found that YUP, the genetic locus responsible for a large portion of floral color variation and previously shown to be important in bee interactions with other Mimulus species, also played an important role in this novel attraction. These results together suggest that the attraction of new pollinators to hybrid plants could be an underexplored avenue for pollinator shift and speciation.

Angiosperm flowers reached their highest morphological diversity early in their evolutionary history.

Flowers are the complex and highly diverse reproductive structures of angiosperms. Because of their role in sexual reproduction, the evolution of flowers is tightly linked to angiosperm speciation and diversification. Accordingly, the quantification of floral morphological diversity (disparity) among angiosperm subgroups and through time may give important insights into the evolutionary history of angiosperms as a whole. Based on a comprehensive dataset focusing on 30 characters describing floral structure across angiosperms, we used 1201 extant and 121 fossil flowers to measure floral disparity and explore patterns of floral evolution through time and across lineages. We found that angiosperms reached their highest floral disparity in the Early Cretaceous. However, decreasing disparity toward the present likely has not precluded the innovation of other complex traits at other morphological levels, which likely played a key role in the outstanding angiosperm species richness. Angiosperms occupy specific regions of the theoretical morphospace, indicating that only a portion of the possible floral trait combinations is observed in nature. The ANA grade, the magnoliids, and the early-eudicot grade occupy large areas of the morphospace (higher disparity), whereas nested groups occupy narrower regions (lower disparity).

Genome-Wide Association and Prediction of Male and Female Floral Hybrid Potential Traits in Elite Spring Bread Wheat Genotypes.

Hybrid wheat breeding is one of the most promising technologies for further sustainable yield increases. However, the cleistogamous nature of wheat displays a major bottleneck for a successful hybrid breeding program. Thus, an optimized breeding strategy by developing appropriate parental lines with favorable floral trait combinations is the best way to enhance the outcrossing ability. This study, therefore, aimed to dissect the genetic basis of various floral traits using genome-wide association study (GWAS) and to assess the potential of genome-wide prediction (GP) for anther extrusion (AE), visual anther extrusion (VAE), pollen mass (PM), pollen shedding (PSH), pollen viability (PV), anther length (AL), openness of the flower (OPF), duration of floret opening (DFO) and stigma length. To this end, we employed 196 ICARDA spring bread wheat lines evaluated for three years and genotyped with 10,477 polymorphic SNP. In total, 70 significant markers were identified associated to the various assessed traits at FDR ≤ 0.05 contributing a minor to large proportion of the phenotypic variance (8–26.9%), affecting the traits either positively or negatively. GWAS revealed multi-marker-based associations among AE, VAE, PM, OPF and DFO, most likely linked markers, suggesting a potential genomic region controlling the genetic association of these complex traits. Of these markers, Kukri_rep_c103359_233 and wsnp_Ex_rep_c107911_91350930 deserve particular attention. The consistently significant markers with large effect could be useful for marker-assisted selection. Genomic selection revealed medium to high prediction accuracy ranging between 52% and 92% for the assessed traits with the least and maximum value observed for stigma length and visual anther extrusion, respectively. This indicates the feasibility to implement genomic selection to predict the performance of hybrid floral traits with high reliability.

Pollinator-dependent evolution of floral trait combinations in an orchid herb

Abstract Aims As one of the most important agents driving floral evolution, pollinators shape the diversity of flowers in angiosperms. However, most previous studies have only quantified pollinators driving the evolution of a single floral trait, and experimental estimates of the potential role of pollinators in shaping the evolution of floral trait associations are relatively rare. Methods We experimentally identified and estimated the pollinator-mediated directional and correlational selection on single floral traits and trait combinations across 2 years in an orchid species, Spiranthes sinensis. Important Findings Pollinators mediated directional selection for an earlier flowering start date and larger corolla size. Pollinators mediated positive correlational selection on the combinations of floral display traits and negative correlational selection on the combinations of flowering phenology and floral display traits. In addition, the strength of selection differed over time. Our results highlight the potential role of pollinators in driving the evolution of floral trait combinations and suggest that it is necessary to consider floral character functional associations when seeking to understand and predict the evolutionary trajectory of flowers in angiosperms.

Quantifying hummingbird preference for floral trait combinations: The role of selection on trait interactions in the evolution of pollination syndromes.

Darwin recognized the flower's importance for the study of adaptation and emphasized that the flower's functionality reflects the coordinated action of multiple traits. Here we use a multitrait manipulative approach to quantify the potential role of selection acting on floral trait combinations underlying the divergence and maintenance of three related North American species of Silene (Caryophyllaceae). We artificially generated 48 plant phenotypes corresponding to all combinations of key attractive traits differing among the three Silene species (color, height, inflorescence architecture, flower orientation, and corolla-tube width). We quantified main and interaction effects of trait manipulation on hummingbird visitation preference using experimental arrays. The main effects of floral display height and floral orientation strongly influenced hummingbird visitation, with hummingbirds preferring flowers held high above the ground and vertically to the sky. Hummingbirds also prefer traits in a nonadditive manner as multiple two-way and higher order interaction effects were important predictors of hummingbird visitation. Contemporary trait combinations found in hummingbird pollinated S. virginica are mostly preferred. Our study demonstrates the likelihood of pollination syndromes evolving due to selection on trait combinations and highlights the importance of trait interactions in understanding the evolution of complex adaptations.

Using the Literature to Test Pollination Syndromes — Some Methodological Cautions

“Pollination syndromes” are specific combinations of floral traits that are proposed to evolve convergently across angiosperm lineages in response to different types of animal pollinators. In spite of their long history, pollination syndromes have not been tested adequately–they rarely have been examined critically to determine how well they describe floral trait diversity or predict pollinators. In a recent meta-analysis of data from the literature, Rosas-Guerrero et al. (2014) provide a welcome test that draws on insights from past studies. At the same time, their study illustrates several difficulties of meta-analysis approaches in general, and for pollination biology in particular. Here we discuss those difficulties and propose some solutions. We first consider how to gather studies from the literature without introducing unintended bias, such as the old-fashioned method of working backward from cited literature. We next consider how to deal with difficulties that invariably arise when extracting and analyzing often-incomplete information from heterogeneous studies. Finally we discuss issues of interpreting and presenting the results in the most informative manner. We conclude that although Rosas-Guerrero et al. (2014) and other studies such as Ollerton et al. (2009) have arrived at different conclusions about the utility of pollination syndromes, their results are not necessarily incompatible.

Selection of trait combinations through bee and fly visitation to flowers of Polemonium foliosissimum

Pollinators are known to exert natural selection on floral traits, but the extent to which combinations of floral traits are subject to correlational selection (nonadditive effects of two traits on fitness) is not well understood. Over two years, we used phenotypic manipulations of plant traits to test for effects of flower colour, flower shape and their interaction on rates of pollinator visitation to Polemonium foliosissimum. We also tested for correlational selection based on weighting visitation by the amount of conspecific pollen delivered per visit by each category of insect visitor. Although bumblebees were the presumed pollinators, solitary bees and flies contributed substantially (42%) to pollination. In manipulations of one trait at a time, insects visited flowers presenting the natural colour and shape over flowers manipulated to present artificial mutants with either paler colour or a more open or more tubular flower. When both colour and shape were manipulated in combination, selection on both traits arose, with bumblebees responding mainly to colour and flies responding mainly to shape. Despite selection on both floral traits, in a year with many bumblebees, we saw no evidence for correlational selection of these traits. In a year when flies predominated, fly visitation showed a pattern of correlational selection, but not favouring the natural phenotype, and correlational selection was still not detected for expected pollen receipt. These results show that flower colour and shape are subject to pollinator-mediated selection and that correlational selection can be generated based on pollinator visitation alone, but provide no evidence for correlational selection specifically for the current phenotype.

Multimodal Floral Signals and Moth Foraging Decisions

BackgroundCombinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.Methodology/Principal FindingsUsing M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.Conclusions/SignificanceThese results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.

Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids

BackgroundSexually deceptive orchids of the genus Ophrys attract their pollinators, male insects, on a highly specific basis through the emission of odour blends that mimic the female sex pheromone of the targeted species. In this study, we have investigated a contact site between Ophrys arachnitiformis and O. lupercalis, two sympatric orchid species that are usually reproductively isolated via the exploitation of different pollinator "niches", but occasionally hybridise despite their apparent combination of ethological and mechanical isolation barriers. In particular, we have investigated the extent to which these Ophrys hybrids generate "emergent" combinations (i.e. novel and unpredictable from the parents' phenotypes) of floral traits, and how these phenotypic novelties, particularly the odour blends emitted by the flower, could facilitate the invasion of a novel pollinator "niche" and induce the rapid formation of reproductive isolation, a prerequisite for adaptive evolutionary divergence.ResultsOur chemical analyses of floral scents show that the Ophrys F1 hybrids investigated here produce more compounds, significantly different ratios (% of odour compounds in the total blend), as well as new compounds in their floral odour compared to their progenitors. When tested for their attractiveness to the pollinator of each parent orchid species, we found that floral scent extracts of the hybrids triggered less inspecting flights and contacts by the male bees with the scented dummy than those of the parental orchid species. However, a series of additional behavioural bioassays revealed that the novel floral scent of the hybrids was significantly more attractive than either of the two parents to a pollinator species not initially involved in the pollination of any of the parent Ophrys species.ConclusionsCollectively, our results illustrate that the process of hybridisation can lead to the generation of evolutionary novelties, and that novel combinations of floral traits can drive pollinator shifts and rapid reproductive isolation in highly specific plant-pollinator interactions.

MACROEVOLUTIONARY TESTS OF POLLINATION SYNDROMES: A REPLY TO FENSTER ET AL.

Studies of floral ecology and evolution are often centered on the idea that particular floral trait combinations, or syndromes, represent adaptations for particular pollinators. Despite the conceptual importance of pollination syndromes, few macroevolutionary studies have statistically examined the relationship between pollinators and floral traits. Using 15 species of Iochroma, Smith et al. applied phylogenetically structured correlation analyses to test the relationship between floral variation and pollination system, quantified in terms of the importance of major pollinator groups. This study revealed that pollinator shifts are tied to changes in nectar reward and floral display but are not significantly correlated with changes in corolla length or color, contrary to what might be predicted from classical pollination syndromes. Fenster et al. question these findings because our pollinator importance estimates included recently introduced honey bees. To address this concern, we recalculated importance values excluding honey bees and repeated the analyses. We found the same patterns as in our original study with significant correlations between pollinators and nectar reward and display. We conclude that phylogenetic approaches provide essential tools for testing macroevolutionary predictions of pollination syndromes and, by applying these approaches to other radiations, we can refine our understanding of the role of pollinators in floral diversification.

Extreme variation in floral characters and its consequences for pollinator attraction among populations of an Andean cactus

A South American cactus species, Echinopsis ancistrophora (Cactaceae), with dramatic among-population variation in floral traits is presented. Eleven populations of E. ancistrophora were studied in their habitats in northern Argentina, and comparisons were made of relevant floral traits such as depth, stigma position, nectar volume and sugar concentration, and anthesis time. Diurnal and nocturnal pollinator assemblages were evaluated for populations with different floral trait combinations. Remarkable geographical variations in floral traits were recorded among the 11 populations throughout the distribution range of E. ancistrophora, with flower lengths ranging from 4.5 to 24.1 cm. Other floral traits associated with pollinator attraction also varied in a population-specific manner, in concert with floral depth. Populations with the shortest flowers showed morning anthesis and those with the longest flowers opened at dusk, whereas those with flowers of intermediate length opened at unusual times (2300-0600 h). Nectar production varied non-linearly with floral length; it was absent to low (population means up to 15 microL) in short- to intermediate-length flowers, but was high (population means up to 170 microL) in the longest tubed flowers. Evidence from light-trapping of moths, pollen carriage on their bodies and moth scale deposition on stigmas suggests that sphingid pollination is prevalent only in the four populations with the longest flowers, in which floral morphological traits and nectar volumes match the classic expectations for the hawkmoth pollination syndrome. All other populations, with flowers 4.5-15 cm long, were pollinated exclusively by solitary bees. The results suggest incipient differentiation at the population level and local adaptation to either bee or hawkmoth (potentially plus bee) pollination.

Nectar reward and advertisement in hummingbird‐pollinated Silene virginica (Caryophyllaceae)

We tested for an association between nectar and various floral traits and investigated their roles as primary and secondary pollinator attractants in hummingbird-pollinated Silene virginica. Our goal was to gain insight into the mechanisms of pollinator-mediated selection that underlies floral trait divergence within the genus. In a field population of S. virginica, we measured five floral and eight vegetative traits and quantified nectar volume, nectar sugar concentration, and total sugar reward (nectar volume × nectar sugar concentration). All three components of nectar reward were positively correlated to flower size, and nectar volume varied significantly among individuals within the population. To ascertain whether the correlation of specific floral traits with nectar reward influences the behavior of the primary pollinator of S. virginica, the ruby-throated hummingbird, Archilochus colubris, we investigated whether A. colubris preferred the expression of floral traits associated with high nectar volume and total sugar reward. We accomplished this by constructing floral arrays consisting of artificial flowers that had equal nectar quantity and total sugar reward but that differed in petal area and corolla tube diameter, which were positively correlated with nectar quantity and total sugar reward in our field study. In observations of visitation frequencies to the various floral-trait combinations, hummingbirds preferentially visited artificial floral phenotypes with larger petal displays, with the greatest preference for floral phenotypes with both larger petals and wider corolla-tube diameters. This association between primary and secondary floral attractants and hummingbird discrimination of floral features supports the concept that the floral traits of S. virginica reflect pollinator-mediated selection by the principal pollinator.

Intra- and Inter-Plant Level Correlations among Floral Traits in Iris Gracilipes (Iridaceae)

Although the sizes of individual flowers within one plant vary, few studies to date have investigated correlations among floral traits at the intra-plant level. Variations of the pleiotropic genes or linkage disequilibrium of genes, those have been said to create larger correlations between some combinations of traits than others at the inter-plant level, cannot predict intra-plant level correlations. In this study, correlations between several combinations of floral traits, including the number and volume of pollen grains and ovules, were investigated at both intra- and inter-plant levels in Iris gracilipes. The pattern of intra-plant level correlations was similar to that of inter-plant level correlations with some exceptions; correlations between functionally related traits tended to be larger than others at both levels. For example, correlations between sepal and petal size, and between petaloid style and filament length were large at both levels. This may be explained by the genetic and the developmental relationships between some combinations of traits, rather than by (co)variations of the peculiar properties of the individual plants such as genetic variations.

Flower constancy in bumblebees: a test of the trait variability hypothesis

Pollinators often sequentially visit one flower type while bypassing other equally rewarding flower types in the process. Many explanations for this pattern of flower choice in pollinators, known as flower constancy, have been proposed; yet, a sufficient answer to the question of why pollinators are constant still remains elusive. We tested the hypothesis that flower constancy in pollinators is related to the number of traits distinguishing available flowers by measuring the floral selectivity (both constancy and preference) of bumblebees, Bombus impatiens, when artificial flower types differed in either colour only (variation in a single trait) or colour and other floral traits (variation in multiple traits). As expected, bees showed increased degrees of selectivity (constancy and preference) when available flower types differed in colour and other floral traits compared with when available flower types differed in colour only. In addition, bee foraging rates (measured in flowers visited per min) varied inversely with the number of variable floral traits added to colour but not with the number of colours. Together, these results are consistent with the idea that the mechanism underlying flower constancy in bumblebees is a limitation on their ability to effectively search for and/or remember multiple combinations of floral traits at the same time. We discuss the roles of floral-trait variation, flower constancy and pollinator cognitive limitations in the coevolution of flowering plants and their animal pollinators.

Floral isolation betweenAquilegia formosaandAquilegia pubescens

The acquisition of floral nectar spurs is correlated with increased species diversity across multiple clades. We tested whether variation in nectar spurs influences reproductive isolation and, thus, can potentially promote species diversity using two species of Aquilegia, Aquilegia formosa and Aquilegia pubescens, which form narrow hybrid zones. Floral visitors strongly discriminated between the two species both in natural populations and at mixed-species arrays of individual flowers. Bees and hummingbirds visited flowers of A. formosa at a much greater rate than flowers of A. pubescens. Hawkmoths, however, nearly exclusively visited flowers of A. pubescens. We found that altering the orientation of A. pubescens flowers from upright to pendent, like the flowers of A. formosa, reduced hawkmoth visitation by an order of magnitude. In contrast, shortening the length of the nectar spurs of A. pubescens flowers to a length similar to A. formosa flowers did not affect hawkmoth visitation. However, pollen removal was significantly reduced in flowers with shortened nectar spurs. These data indicate that floral traits promote floral isolation between these species and that specific floral traits affect floral isolation via ethological isolation while others affect floral isolation via mechanical isolation.