Plant–animal interactions in suburban environments: implications for floral evolution

Plant interactions with mutualists and antagonists vary remarkably across space, and have played key roles in the ecology and evolution of flowering plants. One dominant form of spatial variation is human modification of the landscape, including urbanization and suburbanization. Our goal was to assess how suburbanization affected plant–animal interactions in Gelsemium sempervirens in the southeastern United States, including interactions with mutualists (pollination) and antagonists (nectar robbing and florivory). Based on differences in plant–animal interactions measured in multiple replicate sites, we then developed predictions for how these differences would affect patterns of natural selection, and we explored the patterns using measurements of floral and defensive traits in the field and in a common garden. We found that Gelsemium growing in suburban sites experienced more robbing and florivory as well as more heterospecific but not conspecific pollen transfer. Floral traits, particularly corolla length and width, influenced the susceptibility of plants to particular interactors. Observational data of floral traits measured in the field and in a common garden provided some supporting but also some conflicting evidence for the hypothesis that floral traits evolved in response to differences in species interactions in suburban vs. wild sites. However, the degree to which plants can respond to any one interactor may be constrained by correlations among floral morphological traits. Taken together, consideration of the broader geographic context in which organisms interact, in both suburban and wild areas, is fundamental to our understanding of the forces that shape contemporary plant–animal interactions and selection pressures in native species.     

Drought and leaf herbivory influence floral volatiles and pollinator attraction

The effects of climate change on species interactions are poorly understood. Investigating the mechanisms by which species interactions may shift under altered environmental conditions will help form a more predictive understanding of such shifts. In particular, components of climate change have the potential to strongly influence floral volatile organic compounds (VOCs) and, in turn, plant–pollinator interactions. In this study, we experimentally manipulated drought and herbivory for four forb species to determine effects of these treatments and their interactions on (1) visual plant traits traditionally associated with pollinator attraction, (2) floral VOCs, and (3) the visitation rates and community composition of pollinators. For all forbs tested, experimental drought universally reduced flower size and floral display, but there were species‐specific effects of drought on volatile emissions per flower, the composition of compounds produced, and subsequent pollinator visitation rates. Moreover, the community of pollinating visitors was influenced by drought across forb species (i.e. some pollinator species were deterred by drought while others were attracted). Together, these results indicate that VOCs may provide more nuanced information to potential floral visitors and may be relatively more important than visual traits for pollinator attraction, particularly under shifting environmental conditions.     

SEPALLATA gene diversification: brave new whorls

SEPALLATA (SEP) genes form an integral part of models that outline the molecular basis of floral organ determination and are hypothesized to act as co-factors with ABCD floral homeotic genes in specifying different floral whorls. The four SEP genes in Arabidopsis function redundantly, but the extent to which SEP genes in other flowering plants function similarly is unknown. Using a recent 113-gene SEP phylogeny as a framework, we find surprising heterogeneity among SEP gene C-terminal motifs, mRNA expression patterns, protein-protein interactions and inferred function. Although some SEP genes appear to function redundantly, others have novel roles in fruit maturation, floral organ specification and plant architecture, and have played a major role in floral evolution of diverse plants.     

Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum

All volatile organic compounds (VOCs) vary quantitatively, yet how such variation affects their ecological roles is unknown. Because floral VOCs are cues for both pollinators and floral antagonists, variation in emission may have major consequences for costs and benefits in plant-pollinator interactions. In Polemonium viscosum, the emission rate for the floral VOC 2-phenylethanol (2PE) spans more than two orders of magnitude. We investigated the ecological and evolutionary impacts of this immense phenotypic variation. The emission rate of 2PE varies independently of nectar rewards and thus is uninformative of profitability. Emission is elevated in flowers that are morphologically vulnerable to ant larcenists, suggesting that chemical deterrence may compensate for weak physical barriers. In nature, plants emitting more 2PE than their neighbors escape ant damage. Flower-damaging ants die when exposed to 2PE in the laboratory, and they avoid high 2PE emitters in the field. High 2PE also reduces bumblebee visitation and pollination, suggesting an ecological cost of defense in pollinator service. However, at more moderate emission rates, 2PE enhances the amount of nectar left in flowers, at no pollination cost. In conclusion, repellency of 2PE is highly sensitive to dosage, giving it a key role in shaping ecological interactions between skypilot plants and their floral visitors.     

Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens

Several floral microbes are known to be pathogenic to plants or floral visitors such as pollinators. Despite the ecological and economic importance of pathogens deposited in flowers, we often lack a basic understanding of how floral traits influence disease transmission. Here, we provide the first systematic review regarding how floral traits attract vectors (for plant pathogens) or hosts (for animal pathogens), mediate disease establishment and evolve under complex interactions with plant mutualists that can be vectors for microbial antagonists. Attraction of floral visitors is influenced by numerous phenological, morphological and chemical traits, and several plant pathogens manipulate floral traits to attract vectors. There is rapidly growing interest in how floral secondary compounds and antimicrobial enzymes influence disease establishment in plant hosts. Similarly, new research suggests that consumption of floral secondary compounds can reduce pathogen loads in animal pollinators. Given recent concerns about pollinator declines caused in part by pathogens, the role of floral traits in mediating pathogen transmission is a key area for further research. We conclude by discussing important implications of floral transmission of pathogens for agriculture, conservation and human health, suggesting promising avenues for future research in both basic and applied biology.     

Petrol exhaust pollution impairs honey bee learning and memory

Volatile organic compounds (VOCs) serve as important infochemicals, mediating several ecological interactions including herbivory and pollination. Atmospheric pollutants including traffic‐related air pollution may impair the detection of VOCs used by insects in insect–plant interactions. We investigated the indirect effect of petrol exhaust pollution on olfactory learning and memory (short and long term) in honey bees. Using appetitive olfactory conditioning, we trained bees to learn one of four floral VOC profiles; linalool, dipentene, myrcene and geranium. VOCs were unpolluted or polluted with exhaust collected from a petrol generator. Exhaust emissions included concentrations of CO (246.07 + 17 ppm), NO (20.50 + 6.90 ppb) and NO2 (20.93 + 0.05 ppb) consistent with those typically encountered in urban areas and near roads. Once bees had learnt the training VOC, we tested whether they could recognise that VOC 1 h, 24 h and 48 h post‐training. Bees took significantly longer to learn polluted VOCs and forgot them faster than unpolluted ones. We also tested the ‘masking’ potential of pollution on floral VOCs. Using gas chromatography mass spectroscopy we noted differences in the chemical profile of polluted versus unpolluted VOCs and tested whether bees could recognise polluted VOCs if trained using unpolluted ones. For several VOCs tested, bees could distinguish between polluted and unpolluted VOCs. Ultimately, our results show that air pollution changes the recognition and retention of floral VOCs by bees which may consequently impact foraging efficiency.     

Molecular mechanisms of floral mimicry in orchids

Deceptive plants do not produce floral rewards, but attract pollinators by mimicking signals of other organisms, such as food plants or female insects. Such floral mimicry is particularly common in orchids, in which flower morphology, coloration and odour play key roles in deceiving pollinators. A better understanding of the molecular bases for these traits should provide new insights into the occurrence, mechanisms and evolutionary consequences of floral mimicry. It should also reveal the molecular bases of pollinator-attracting signals, in addition to providing strategies for manipulating insect behaviour in general. Here, we review data on the molecular bases for traits involved in floral mimicry, and we describe methodological advances helpful for the functional evaluation of key genes.     

Functional analyses of a flavonol synthase–like gene from Camellia nitidissima reveal its roles in flavonoid metabolism during floral pigmentation

The flavonoids metabolic pathway plays central roles in floral coloration, in which anthocyanins and flavonols are derived from common precursors, dihydroflavonols. Flavonol synthase (FLS) catalyses dihydroflavonols into flavonols, which presents a key branch of anthocyanins biosynthesis. The yellow flower of Camellia nitidissima Chi. is a unique feature within the genus Camellia, which makes it a precious resource for breeding yellow camellia varieties. In this work, we characterized the secondary metabolites of pigments during floral development of C. nitidissima and revealed that accumulation of flavonols correlates with floral coloration. We first isolated CnFLS1 and showed that it is a FLS of C. nitidissima by gene family analysis. Second, expression analysis during floral development and different floral organs indicated that the expression level of CnFLS1 was regulated by developmental cues, which was in agreement with the accumulating pattern of flavonols. Furthermore, over-expression of CnFLS1 in Nicotiana tabacum altered floral colour into white or light yellow, and metabolic analysis showed significant increasing of flavonols and reducing of anthocyanins in transgenic plants. Our work suggested CnFLS1 plays critical roles in yellow colour pigmentation and is potentially a key point of genetic engineering toward colour modification in Camellia.     

Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem

Pathogens can alter host phenotypes in ways that influence interactions between hosts and other organisms, including insect disease vectors. Such effects have implications for pathogen transmission, as well as host exposure to secondary pathogens, but are not well studied in natural systems, particularly for plant pathogens. Here, we report that the beetle‐transmitted bacterial pathogen Erwinia tracheiphila – which causes a fatal wilt disease – alters the foliar and floral volatile emissions of its host (wild gourd, Cucurbita pepo ssp. texana) in ways that enhance both vector recruitment to infected plants and subsequent dispersal to healthy plants. Moreover, infection by Zucchini yellow mosaic virus (ZYMV), which also occurs at our study sites, reduces floral volatile emissions in a manner that discourages beetle recruitment and therefore likely reduces the exposure of virus‐infected plants to the lethal bacterial pathogen – a finding consistent with our previous observation of dramatically reduced wilt disease incidence in ZYMV‐infected plants.     

Evolution of floral morphology and pollination system in Bignonieae (Bignoniaceae)

The radiation of angiosperms is associated with shifts among pollination modes that are thought to have driven the diversification of floral forms. However, the exact sequence of evolutionary events that led to such great diversity in floral traits is unknown for most plant groups. Here, we characterize the patterns of evolution of individual floral traits and overall floral morphologies in the tribe Bignonieae (Bignoniaceae). We identified 12 discrete traits that are associated with seven floral types previously described for the group and used a penalized likelihood tree of the tribe to reconstruct the ancestral states of those traits at all nodes of the phylogeny of Bignonieae. In addition, evolutionary correlations among traits were conducted using a maximum likelihood approach to test whether the evolution of individual floral traits followed the correlated patterns of evolution expected under the "pollination syndrome" concept. The ancestral Bignonieae flower presented an Anemopaegma-type morphology, which was followed by several parallel shifts in floral morphologies. Those shifts occurred through intermediate stages resulting in mixed floral morphologies as well as directly from the Anemopaegma-type morphology to other floral types. Positive and negative evolutionary correlations among traits fit patterns expected under the pollination syndrome perspective, suggesting that interactions between Bignonieae flowers and pollinators likely played important roles in the diversification of the group as a whole.     

Leaf herbivory increases floral fragrance in male but not female Cucurbita pepo subsp. texana (Cucurbitaceae) flowers

Mutualisms are key interactions that affect population dynamics and structure communities, but the extent to which mutualists can attract potential partners may depend on community context. Many studies have shown that leaf herbivory reduces pollinator visitation and have focused on reduced floral visual display and rewards as potential mechanisms. However, olfactory display plays a critical role in mediating interactions between plants, herbivores, and pollinators. We simulated leaf damage in Cucurbita pepo subsp. texana and measured fragrance emission and other floral characters of both male and female flowers. Contrary to our expectations, damage increased fragrance production, but only in male flowers. Female flowers, which were bigger and produced more fragrance than males, were unaffected by leaf damage. The greatest increase in floral fragrance compounds was in the terpenoids, which we hypothesize could be byproducts of defensively induced cucurbitacins, or they may function defensively themselves. In summary, this study is the first to demonstrate changes in floral fragrance due to leaf damage. Such changes in floral fragrance following herbivory may be a critical and overlooked mechanism mediating interactions between plants, herbivores, and pollinators.     

Variation in highbush blueberry floral volatile profiles as a function of pollination status, cultivar, time of day and flower part: implications for flower visitation by bees

Background and Aims

Studies of the effects of pollination on floral scent and bee visitation remain rare, particularly in agricultural crops. To fill this gap, the hypothesis that bee visitation to flowers decreases after pollination through reduced floral volatile emissions in highbush blueberries, Vaccinium corymbosum, was tested. Other sources of variation in floral emissions and the role of floral volatiles in bee attraction were also examined.

Methods

Pollinator visitation to blueberry flowers was manipulated by bagging all flowers within a bush (pollinator excluded) or leaving them unbagged (open pollinated), and then the effect on floral volatile emissions and future bee visitation were measured. Floral volatiles were also measured from different blueberry cultivars, times of the day and flower parts, and a study was conducted to test the attraction of bees to floral volatiles.

Key Results

Open-pollinated blueberry flowers had 32 % lower volatile emissions than pollinator-excluded flowers. In particular, cinnamyl alcohol, a major component of the floral blend that is emitted exclusively from petals, was emitted in lower quantities from open-pollinated flowers. Although, no differences in cinnamyl alcohol emissions were detected among three blueberry cultivars or at different times of day, some components of the blueberry floral blend were emitted in higher amounts from certain cultivars and at mid-day. Field observations showed that more bees visited bushes with pollinator-excluded flowers. Also, more honey bees were caught in traps baited with a synthetic blueberry floral blend than in unbaited traps.

Conclusions

Greater volatile emissions may help guide bees to unpollinated flowers, and thus increase plant fitness and bee energetic return when foraging in blueberries. Furthermore, the variation in volatile emissions from blueberry flowers depending on pollination status, plant cultivar and time of day suggests an adaptive role of floral signals in increasing pollination of flowers.     

Nocturnal emission and post-pollination change of floral scent in the leafflower tree,Glochidion rubrum,exclusively pollinated by seed-parasitic leafflower moths

Many insect-pollinated plants use floral scent signals to attract and guide the effective pollinators, and temporal patterns of their floral scent emission may be tuned to respond to the pollinator's activity and pollination status. In the intimate nursery pollination mutualism between monoecious Glochidion trees (Phyllanthaceae) and Epicephala moths (Gracillariidae), floral scent signals mediate species-specific interactions and influence the moth's efficient pollen-collecting and pollen-depositing behaviors on male and female flowers, respectively. We tested the hypotheses that both sexes of flowers of Epicephala-pollinated Glochidion rubrum exhibit a diel pattern of scent emission matching the activity period of the nocturnally active pollinator, and that female flowers change the chemical signal after pollination to reduce further visits and oviposition by the pollinator. We investigated the diel change of floral scent emissions during two consecutive days and the influence of pollination on the floral scent by conducting hand-pollinations in the field. The total scent emission of male and female flowers was higher at night than in the day, which would be expected from the nocturnal visitations of Epicephala moths. Some compounds exhibited a clear nocturnal emission rhythm. Hand-pollination experiments revealed that emission of two compounds, nerolidol and eugenol, drastically decreased in pollinated flowers, suggesting that these compounds may function as key attractants for the pollinator; however, the total scent emission of the female flower was not influenced by hand-pollination. The pattern of the floral scent emission of G. rubrum may be optimized to attract nocturnal pollinators and reduce oviposition.     

Evolutionary breakdown of distyly to homostyly is accompanied by reductions of floral scent in Primula oreodoxa

Reproductive traits that function in pollinator attraction may be reduced or lost during evolutionary transitions from outcrossing to selfing. Although floral scent plays an important role in attracting pollinators in outcrossing species, few studies have investigated associations between floral scent variation and intraspecific mating system transitions. The breakdown of distyly to homostyly represents a classic example of a shift from outcrossing to selfing and provides an opportunity to test whether floral fragrances have become reduced and/or changed in composition with increased selfing. Here, we evaluate this hypothesis by quantifying floral volatiles using gas chromatography-mass spectrometry in two distylous and four homostylous populations of Primula oreodoxa Franchet, a perennial herb from SW China. Our analysis revealed significant variation of volatile organic compounds (VOCs) among populations of P. oreodoxa. Although there was no difference in VOCs between floral morphs in distylous populations as predicted, we detected a substantial reduction in VOC emissions and the average number of scent compounds in homostylous compared with distylous populations. A total of 12 compounds, mainly monoterpenoids and sesquiterpenoids, distinguished homostylous and distylous morphs; of these, (E)-β-ocimene was the most important in contributing to the difference in volatiles, with significantly lower emissions in homostyles. Our findings support the hypothesis that the transition from outcrossing to selfing is accompanied by the loss of floral volatiles. The modification to floral fragrances in P. oreodoxa associated with mating system change might occur because high selfing rates in homostylous populations result in relaxed selection for floral attractiveness.     

Genome-wide analysis reveals widespread roles for RcREM genes in floral organ development in Rosa chinensis

Members of the REM (Reproductive Meristem) gene family are expressed primarily in reproductive meristems and floral organs. However, their evolution and their functional profiles in flower development remain poorly understood. Here, we performed genome-wide identification and evolutionary analysis of the REM gene family in Rosaceae. This family has been greatly expanded in rose (Rosa chinensis) compared to other species, primarily through tandem duplication. Expression analysis revealed that most RcREM genes are specifically expressed in reproductive organs and that their specific expression patterns are dramatically altered in rose plants with mutations affecting floral organs. Protein-protein interaction analysis indicated that RcREM14 interact with RcAP1 (one of the homology of A class genes in ABCDE model), highlighting the roles of RcREM genes in floral organ identity. Finally, co-expression network analysis indicated that RcREM genes are co-expressed with a high proportion of key genes that regulate flowering time, floral organ development, and cell proliferation and expansion in R. chinensis.     

DECONSTRUCTING HETEROSTYLY: THE EVOLUTIONARY ROLE OF INCOMPATIBILITY SYSTEM,POLLINATORS, AND FLORAL ARCHITECTURE

Darwin's early work on heterostyly and related style polymorphisms (the presence of two or three style morphs within a population) generated much interest to understand how precise interactions between ecological and genetic mechanisms influence the evolution of floral diversity. Here we tested three key hypotheses proposed to explain the evolution of heterostyly: (i) the presence of self‐incompatibility; (ii) the role of pollinators in promoting dissasortative mating; and (iii) floral architecture, which restricts pollinators’ movements and ensures more exact pollen deposition on their bodies. We combined data from experiments, field observations, and published studies to test whether evolution of style polymorphism in Narcissus is driven by the incompatibility system, pollinator guilds, or floral architecture, within a phylogenetic framework. Neither differences in pollinator environment nor the presence of genetic self‐incompatibility were correlated with presence of style polymorphism. However, our results indicate that the evolution of style polymorphism was driven by the presence of a narrow and long floral tube.