Search

PremiseCapparis spinosa is a widespread charismatic plant, in which the nocturnal floral habit contrasts with the high visitation by diurnal bees and the pronounced scarcity of hawkmoths. To resolve this discrepancy and elucidate floral evolution of C. spinosa, we analyzed the intrafloral patterns of visual and olfactory cues in relation to the known sensory biases of the different visitor guilds (bees, butterflies, and hawkmoths). MethodsWe measured the intrafloral variation of scent, reflectance spectra, and colorimetric properties according to three guilds of known visitors of C. spinosa. Additionally, we sampled visitation rates using a motion-activated camera. ResultsCarpenter bees visited the flowers eight times more frequently than nocturnal hawkmoths, at dusk and in the following morning. Yet, the floral headspace of C. spinosa contained a typical sphingophilous scent with high emission rates of certain monoterpenes and amino-acid derived compounds. Visual cues included a special case of multisensory nectar guide and color patterns conspicuous to the visual systems of both hawkmoths and bees. ConclusionsThe intrafloral patterns of sensory stimuli suggest that hawkmoths have exerted strong historical selection on C. spinosa. Our study revealed two interesting paradoxes: (a) the flowers phenotypically biased towards the more inconsistent pollinator; and (b) floral display demands an abundance of resources that seems maladaptive in the habitats of C. spinosa. The transition to a binary pollination system accommodating large bees has not required phenotypic changes, owing to specific eco-physiological adaptations, unrelated to pollination, which make this plant an unusual case in pollination ecology., American Journal of Botany, 110 (1), ISSN:1914-2016, ISSN:0002-9122

PremiseGenetic variation influences the potential for evolution to rescue populations from impacts of environmental change. Most studies of genetic variation in fitness-related traits focus on either vegetative or floral traits, with few on floral scent. How vegetative and floral traits compare in potential for adaptive evolution is poorly understood.MethodsWe measured variation across source populations, planting sites, and genetic families for vegetative and floral traits in a hybrid zone. Seeds from families of Ipomopsis aggregata, I. tenuituba, and F1 and F2 hybrids of the two species were planted into three common gardens. Measured traits included specific leaf area (SLA), trichomes, water-use efficiency (WUE), floral morphology, petal color, nectar, and floral volatiles.ResultsVegetative traits SLA and WUE varied greatly among planting sites, while showing weak or no genetic variation among source populations. Specific leaf area and trichomes responded plastically to snowmelt date, and SLA exhibited within-population genetic variation. All aspects of floral morphology varied genetically among source populations, and corolla length, corolla width, and sepal width varied genetically within populations. Heritability was not detected for volatiles due to high environmental variation, although one terpene had high evolvability, and high emission of two terpenes, a class of compounds emitted more strongly from the calyx than the corolla, correlated genetically with sepal width. Environmental variation across sites was weak for floral morphology and stronger for volatiles and vegetative traits. The inheritance of three of four volatiles departed from additive.ConclusionsResults indicate stronger genetic potential for evolutionary responses to selection in floral morphology compared with scent and vegetative traits and suggest potentially adaptive plasticity in some vegetative traits.

—Oenotherasect.Pachylophushas proven to be a valuable system in which to study plant-insect coevolution and the drivers of variation in floral morphology and scent. Current species circumscriptions based on morphological characteristics suggest that the section consists of five species, one of which is subdivided into five subspecies. Previous attempts to understand species (and subspecies) relationships at a molecular level have been largely unsuccessful due to high levels of incomplete lineage sorting and limited phylogenetic signal from slowly evolving gene regions. In the present study, target enrichment was used to sequence 322 conserved protein-coding nuclear genes from 50 individuals spanning the geographic range ofOenotherasect.Pachylophus, with species trees inferred using concatenation and coalescent-based methods. Our findings concur with previous research in suggesting thatO. psammophilaandO. harringtoniiare nested within a paraphyleticOenothera cespitosa. By contrast, our results show clearly that the two annual species (O. cavernaeandO. brandegeei) did not arise from theO. cespitosalineage, but rather from a common ancestor ofOenotherasect.Pachylophus. Budding speciation as a result of edaphic specialization appears to best explain the evolution of the narrow endemic speciesO. harringtoniiandO. psammophila. Complete understanding of possible introgression among subspecies ofO. cespitosawill require broader sampling across the full geographical and ecological ranges of these taxa.

The obligate pollination mutualism between Yucca and yucca moths is a classical example of coevolution. Oviposition and active pollination by female yucca moths occur at night when Yucca flowers are open and strongly scented. Thus, floral volatiles have been suggested as key sensory signals attracting yucca moths to their host plants, but no bioactive compounds have yet been identified. In this study, we showed that both sexes of the pollinator moth Tegeticula yuccasella are attracted to the floral scent of the host Yucca filamentosa. Chemical analysis of the floral headspace from six Yucca species in sections Chaenocarpa and Sarcocarpa revealed a set of novel tetranorsesquiterpenoids putatively derived from (E)-4,8-dimethyl-1,3,7-nonatriene. Their structure elucidation was accomplished by NMR analysis of the crude floral scent sample of Yucca treculeana along with GC/MS analysis and confirmed by total synthesis. Since all these volatiles are included in the floral scent of Y. filamentosa, which has been an important model species for understanding the pollination mutualism, we name these compounds filamentolide, filamentol, filamental, and filamentone. Several of these compounds elicited antennal responses in pollinating (Tegeticula) and non-pollinating (Prodoxus) moth species upon stimulation in electrophysiological recordings. In addition, synthetic (Z)-filamentolide attracted significant numbers of both sexes of two associated Prodoxus species in a field trapping experiment. Highly specialized insect-plant interactions, such as obligate pollination mutualisms, are predicted to be maintained through "private channels" dictated by specific compounds. The identification of novel bioactive tetranorsesquiterpenoids is a first step in testing such a hypothesis in the Yucca-yucca moth interaction.

Floral scent is a complex trait that mediates many plant-insect interactions, but our understanding of how floral scent variation evolves, either independently or in concert with other traits, remains limited. Assessing variation in floral scent at multiple levels of biological organization and comparing patterns of variation in scent to variation in other floral traits can contribute to our understanding of how scent variation evolves in nature.We used a greenhouse common garden experiment to investigate variation in floral scent at three scales-within plants, among plants, and among populations-and to determine whether scent, alone or in combination with morphology and rewards, contributes to population differentiation in Oenothera cespitosa subsp. marginata. Its range spans most of the biomes in the western United States, such that variation in both the abiotic and biotic environment could contribute to trait variation.Multiple analytical approaches demonstrated substantial variation among and within populations in compound-specific and total floral scent measures. Overall, populations were differentiated in morphology and reward traits and in scent. Across populations, coupled patterns of variation in linalool, leucine-derived compounds, and hypanthium length are consistent with a long-tongued moth pollination syndrome.The considerable variation in floral scent detected within populations suggests that, similar to other floral traits, variation in floral scent may have a heritable genetic component. Differences in patterns of population differentiation in floral scent and in morphology and rewards indicate that these traits may be shaped by different selective pressures.

Oenothera sect. Calylophus is a North American group of 13 recognized taxa in the evening primrose family (Onagraceae) with an evolutionary history that may include independent origins of bee pollination, edaphic endemism, and permanent translocation heterozygosity. Like other groups that radiated relatively recently and rapidly, taxon boundaries within Oenothera sect. Calylophus have remained challenging to circumscribe. In this study, we used target enrichment, flanking noncoding regions, gene tree/species tree methods, tests for gene flow modified for target-enrichment data, and morphometric analysis to reconstruct phylogenetic hypotheses, evaluate current taxon circumscriptions, and examine character evolution in Oenothera sect. Calylophus. Because sect. Calylophus comprises a clade with a relatively restricted geographic range, we were able to extensively sample across the range of geographic, edaphic, and morphological diversity in the group. We found that the combination of exons and flanking noncoding regions led to improved support for species relationships. We reconstructed potential hybrid origins of some accessions and note that if processes such as hybridization are not taken into account, the number of inferred evolutionary transitions may be artificially inflated. We recovered strong evidence for multiple evolutionary origins of bee pollination from ancestral hawkmoth pollination, edaphic specialization on gypsum, and permanent translocation heterozygosity. This study applies newly emerging techniques alongside dense infraspecific sampling and morphological analyses to effectively reconstruct the recalcitrant history of a rapid radiation. [Gypsum endemism; Oenothera sect. Calylophus; Onagraceae; phylogenomics; pollinator shift; recent radiation; target enrichment.]

Organismal traits often influence fitness via interactions with multiple species. That selection is not necessarily predictable from pairwise interactions, such as when interactions occur during different life cycle stages. Theoretically, directional selection during two sequential episodes (e.g., pollination and seed survival) can generate quadratic or correlational selection for a set of traits that passes both selective filters. We compared strength of selection during pollination versus seed predation in the field and tested whether interactions with multiple species give rise to nonlinear selection on floral traits. We planted common gardens with seeds of two species of

Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health—growth, survivorship, fecundity—across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata , interacting with a rare plant, Oenothera harringtonii , that is polymorphic for the common floral volatile ( R )-(−)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant–pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.

Several monoecious species of palms have developed complex strategies to promote cross-pollination, including the production of large quantities of floral resources and the emission of scents that are attractive to pollinators. Syagrus coronata constitutes an interesting model with which to understand the evolution of plant reproductive strategies in a monoecious species adapted to seasonally dry forests. We monitored blooming phenology over 1 year, during which we also collected and identified floral visitors and putative pollinators. We identified potential floral visitor attractants by characterizing the scent composition of inflorescences as well as of peduncular bracts, during both male and female phases, and the potential for floral thermogenesis. Syagrus coronata produces floral resources throughout the year. Its inflorescences are predominantly visited by a diverse assortment of small-sized beetles, whose richness and abundance vary throughout the different phases of anthesis. We did not find evidence of floral thermogenesis. A total of 23 volatile compounds were identified in the scent emitted by the inflorescences, which did not differ between male and female phases; whereas the scent of the peduncular bracts was composed of only 4-methyl guaiacol, which was absent in inflorescences. The composition of floral scent chemistry indicates that this palm has evolved strategies to be predominantly pollinated by small-sized weevils. Our study provides rare evidence of a non-floral scent emitting structure involved in pollinator attraction, only the second such case specifically in palms. The peculiarities of the reproductive strategy of S. coronata might play an important role in the maintenance of pollination services and pollen dispersion.

Although visual and olfactory floral signals attract pollinators from a distance, at the flower’s threshold, pollinators can use floral humidity as an index cue for nectar presence. We evaluate the role of floral humidity in theDatura wrightii-Manduca sextanocturnal pollination system. In addition to our finding thatM. sextashows strong innate attraction toward humid flowers, we identify the hygrosensing sensillum on their antennae, demonstrate its extreme sensitivity to minute changes in RH, and observe the elimination of moths’ behavioral preference towards humid flowers following experimental occlusion of the sensilla. Despite Manduca’s attraction toward humid flowers, we find that floral humidity is not a reliable cue for nectar presence in this system. While Datura floral headspace sustains an enormous humidity gradient, it is not a consequence of nectar evaporation, but an outcome of gas exchange through floral stomata and is decoupled from nectar presence. Using interdisciplinary tools, we demonstrate the function of floral humidity as an attractive signal, not a cue, in this pollination system, thus showcasing an underappreciated modality by which flowers may manipulate their visitors.

To avoid inbreeding depression, plants have evolved diverse breeding systems to favor outcrossing, such as self-incompatibility. However, changes in biotic and abiotic conditions can result in selective pressures that lead to a breakdown in self-incompatibility. The shift to increased selfing is commonly associated with reduced floral features, lower attractiveness to pollinators, and increased inbreeding. We tested the hypothesis that the loss of self-incompatibility, a shift to self-fertilization (autogamy), and concomitant evolution of the selfing syndrome (reduction in floral traits associated with cross-fertilization) will lead to increased inbreeding and population differentiation in Oenothera primiveris. Across its range, this species exhibits a shift in its breeding system and floral traits from a self-incompatible population with large flowers to self-compatible populations with smaller flowers.We conducted a breeding system assessment, evaluated floral traits in the field and under controlled conditions, and measured population genetic parameters using RADseq data.Our results reveal a bimodal transition to the selfing syndrome from the west to the east of the range of O. primiveris. This shift includes variation in the breeding system and the mating system, a reduction in floral traits (flower diameter, herkogamy, and scent production), a shift to greater autogamy, reduced genetic diversity, and increased inbreeding.The observed variation highlights the importance of range-wide studies to understand breeding system variation and the evolution of the selfing syndrome within populations and species.

To meet energetic and osmotic demands, animals make dynamic foraging decisions about food quality and quantity. In the wild, foraging animals may be forced to consume a less preferred or sub-optimal food source for long periods of time. Few choice feeding assays in laboratory settings approximate such contingencies. In this study the foraging behaviors of the hawkmoth Manduca sexta were measured when adult moths were placed within different relative humidity (RH) environments (20%, 40%, 60% and 80% RH) and provided with only one of the following experimental nectars: 0% (water), 12% or 24 % w/V sucrose solutions. Overall, ambient humidity influenced survivorship and foraging behaviors. Moth survivorship increased at higher ambient humidity regardless of experimental nectar. Moths that had access to experimental nectar imbibed large volumes of fluid regardless of what nectar was offered when placed at the lowest humidity (20% RH). However, when placed at the highest humidity (80% RH), moths imbibed higher volumes of fluid when given access to experimental nectar with sucrose in comparison with water. RH also influenced daily foraging behaviors: peak nectar consumption occurred earlier at lower RH levels. Consistent with previous studies in which moths could choose among nectar solutions, total energy intake was not affected by ambient RH under no-choice conditions. However, the proportion of time spent foraging and total energy consumption were significantly reduced across all RH levels in no-choice assays, when compared with previous studies of choice assays under the same conditions. Our results show that even when M. sexta moths are presented with limited options, they can alter their foraging behavior in response to environmental changes, enabling them to meet osmotic and/or energetic demands.

A recent claim that evening primrose flowers adaptively secrete nectar in response to vibrations from hovering bees lacks supporting evidence. The authors fail to demonstrate that bees can access the concealed nectar and that their visits enhance plant fitness. Reanalysis of the authors' data raises additional concerns about their conclusions.

The attention of the global pollination community has been drawn to food safety and other ecosystem services provided by pollinators, in light of decline in social bee populations. Despite intensified research on bees, recent studies have revealed important contributions of flies to pollination success, reproductive isolation and floral diversification. Diptera is a highly diverse insect order, comprising over 125,000 described species in 110 families and representing a broad spectrum of ecological niches beyond the well-known agricultural pests and blood-feeding vectors of human and animal diseases. Flies are most appreciated as generalized pollinators in alpine habitats (anthomyiids and tachinids) and as specialized pollinators in brood-site deceptive plants that mimic fungi (drosophilids), feces (muscids) or carrion (sarcophagids and calliphorids). Syrphid and bombyliid flies visit many of the same flowers as bees and butterflies do, but with different impacts on plant fitness. Guilds of South African plants have evolved specialized relationships with long-tongued nemestrinid and tabanid flies, thanks to geographic isolation and climatic stability. Studies in Japan highlight the evolution of another plant guild, pollinated by sciarid and mycetophilid fungus gnats, whereas Zygothrica flies (Drosophilidae) pollinate mushroom-like Dracula orchids in Andean cloud forests.

The olfactory cues used by various animals to detect and identify food items often include volatile organic compounds (VOCs) produced by food-associated microorganisms. Microbial VOCs have potential as lures to trap animal pests, including insect crop pests. This study investigated microorganisms whose VOCs are attractive to natural populations of the spotted wing drosophila (SWD), an invasive insect pest of ripening fruits. The microorganisms readily cultured from wild SWD and SWD-infested fruits included yeasts, especially Hanseniaspora species, and various bacteria, including Proteobacteria (especially Acetobacteraceae and Enterobacteriaceae) and Actinobacteria. Traps in a raspberry planting that were baited with cultures of Hanseniaspora uvarum, H. opuntiae and the commercial lure Scentry trapped relatively high numbers of both SWD and non-target drosophilids. The VOCs associated with these baits were dominated by ethyl acetate and, for yeasts, other esters. By contrast, Gluconobacter species (Acetobacteraceae), whose VOCs were dominated by acetic acid and acetoin and lacked detectable ethyl acetate, trapped 60-75% fewer SWD but with very high selectivity for SWD. VOCs of two other taxa tested, the yeast Pichia sp. and Curtobacterium sp. (Actinobacteria), trapped very few SWD or other insects. Our demonstration of among-microbial variation in VOCs and their attractiveness to SWD and non-pest insects under field conditions provides the basis for improved design of lures for SWD management. Further research is required to establish how different microbial VOC profiles may function as reliable cues of habitat suitability for fly feeding and oviposition, and how this variation maps onto among-insect species differences in habitat preference.

Chemosensory communication between flowers and pollinators is a fundamental component of terrestrial biodiversity, given the importance of olfaction to foraging animals. In this respect, exploring chemically mediated interspecific interactions in natural assemblies may provide novel insights into the ecofunctional significance of volatile organic compounds (VOCs) for plant–insect co‐evolution. However, multispecies datasets of associations between plant semiochemicals and arthropods are still very rare and tend to lack community context. Here, we present the first insect–floral VOC meta‐network using plant–pollinator visitation data and the plants’ floral scent blends, collected in a Mediterranean scrubland. We assembled the insect–VOC meta‐network by substituting each plant species in the plant–pollinator network with the blend of VOCs it emits. Furthermore, we identified the modules of the network that is the most densely connected insect–VOC groups. After describing the role of the species in the network, we focused on the bees of the community, and by building phylogenetically informed GLS models, we found the species traits predicting the degree of chemical specialization. Modularity analysis of the meta‐network revealed tight associations between several classes of VOCs and pollinator groups. Linkage patterns suggest positive associations between (a) Megachilidae bees and sesquiterpenes, (b) Apidae and Andrenidae bees and benzenoids/phenylpropanoids, and (c) wasps, C6 green‐leaf volatiles and specific terpenoids. Benzenoids were found to be the least influential and most specialized chemical class in the community, whereas sesquiterpenes represented the most influential one. Furthermore, the degree of chemical generalization of the bees in the meta‐network was significantly associated with their ecological generalization, body mass and phenology, whereas their contribution to the network's structure was related to their level of sociality. Synthesis. Our findings help to disclose the ecofunctional significance of the floral volatile landscape and contribute novel testable hypotheses on the behavioural trends and chemical niches of pollinators in a natural community. The insect–volatilome meta‐network is thus shown to be advantageous for detecting and visualizing patterns of chemically mediated interspecific interactions. Given the ubiquity of chemosensory biocommunication, our approach can be applied for investigating various types of ecological interactions in community contexts.

The study of floral trait diversity has a long history due to its role in angiosperm diversification. While many studies have focused on visual traits including morphology and color, few have included floral scent despite its importance in pollination. Of the studies that have included floral scent, sampling has been limited and rarely explores variation at the population level. We studied geographic variation in the flowers of Oenothera harringtonii, a rare plant endemic to a vulnerable shortgrass prairie habitat, whose population structure and conservation status are well studied. The self-incompatible flowers of O. harringtonii open at dusk, produce nectar and a strong fragrance, and are pollinated by hawkmoths. We collected floral trait (morphology, scent chemistry and emission rates) data from 650 individuals from 19 wild populations to survey floral variation across the entire range of this species. Similarly, we collected floral data from 49 individuals grown in a greenhouse common garden, to assess whether variation observed in the field is consistent when environment factors (temperature, watering regime, soil) are standardized. We identified 35 floral volatiles representing 5 biosynthetic classes. Population differentiation was stronger for floral scent chemistry than floral morphology. (R)-(-)-linalool was the most important floral trait differentiating populations, exhibiting clinal variation across the distribution of O. harringtonii without any correlated shifts in floral morphology. Populations in the north and west produced (R)-(-)-linalool consistently, those in the east and south largely lacked it, and populations at the center of the distribution were polymorphic. Floral scent emissions in wild populations varied across four years but chemical composition was largely consistent over time. Similarly, volatile emission rates and chemical composition in greenhouse-grown plants were consistent with those of wild populations of origin. Our data set, which represents the most extensive population-level survey of floral scent to date, indicates that such sampling may be needed to capture potentially adaptive geographic variation in wild populations.

Floral scent is a key communication channel between plants and pollinators. However,the contributions of environment and phylogeny to floral scent composition remain poorly understood. In this study, we characterized interspecific variation of floral scent composition in the genus Jaborosa Juss. (Solanaceae) and, using an ecological niche modelling approach (ENM), we assessed the environmental variables that exerted the strongest influence on floral scent variation, taking into account pollination mode and phylogenetic relationships. Our results indicate that two major evolutionary themes have emerged: (i) a ?warm Lowland Subtropical nectar-rewarding clade? with large white hawkmoth pollinated flowers that emit fragrances dominated by oxygenated aromatic or sesquiterpenoid volatiles, and (ii) a ?cool-temperate brood-deceptive clade? of largely fly-pollinated species found at high altitudes (Andes) or latitudes (Patagonian Steppe) that emit foul odors including cresol, indole and sulfuric volatiles. The joint consideration of floral scent profiles, pollination mode, and geoclimatic context helped us to disentangle the factors that shaped floral scent evolution across ?pollinator climates? (geographic differences in pollinator abundance or preference). Our findings suggest that the ability of plants in the genus Jaborosa to colonize newly formed habitats during Andean orogeny was associated with striking transitions in flower scent composition that trigger specific odor-driven behaviors in nocturnal hawkmoths and saprophilous fly pollinators. Fil: More, Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Soteras, María Florencia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Ibañez, Ana Clara. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Dötterl, Stefan. Paris-lodron-university Of Salzburg; Austria Fil: Cocucci, Andrea Aristides. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Raguso, Robert A.. Cornell University, Dept. Of Neurobiology And Behavior; Estados Unidos

Oenothera sect. Calylophus is a North American group of 13 recognized taxa in the evening primrose family (Onagraceae) with an evolutionary history that may include independent origins of bee pollination, edaphic endemism, and permanent translocation heterozygosity. Like other groups that radiated relatively recently and rapidly, taxon boundaries within Oenothera sect. Calylophus have remained challenging to circumscribe. In this study, we used target enrichment, flanking non-coding regions, summary coalescent methods, tests for gene flow modified for target-enrichment data, and morphometric analysis to reconstruct phylogenetic hypotheses, evaluate current taxon circumscriptions, and examine character evolution in Oenothera sect. Calylophus. Because sect. Calylophus comprises a clade with a relatively restricted geographic range, we were able to extensively sample across the range of geographic and morphological diversity in the group. We found that the combination of exons and flanking non-coding regions led to improved support for species relationships. We reconstructed potential hybrid origins of some accessions and note that if processes such as hybridization are not taken into account, the number of inferred evolutionary transitions may be artificially inflated. We recovered strong evidence for multiple origins of the evolution of bee pollination from ancestral hawkmoth pollination, the evolution of edaphic specialization on gypsum, and permanent translocation heterozygosity. This study applies newly emerging techniques alongside dense infraspecific sampling and morphological analyses to effectively address a relatively common but recalcitrant problem in evolutionary biology.

BackgroundPlant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(-)-linalool; some plants emit (R)-(-)-linalool (linalool+ plants) while others do not (linalool-plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(-)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool-plants.ResultsThree clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(-)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(-)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants.ConclusionsBy using a naturally occurring polymorphism and comparing different tissues, we were able to identify genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool-plants suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(-)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.

The ecological dynamics of co-flowering communities are largely mediated by pollinators. However, current understanding of pollinator-mediated interactions primarily relies on how co-flowering plants influence attraction of shared pollinators, and much less is known about plant–plant interactions that occur via heterospecific pollen (HP) transfer. Invaded communities in particular can be highly affected by the transfer of alien pollen, but the strength, drivers and fitness consequences of these interactions at a community scale are not well understood. Here we analyse HP transfer networks in nine coastal communities in the Yucatan Mexico that vary in the relative abundance of invasive flowers to evaluate how HP donation and receipt varies between native and alien plants. We further evaluate whether HP donation and receipt are mediated by floral traits (e.g. display, flower size) or pollinator visitation rate. Finally, we evaluated whether post-pollination success (proportion of pollen tubes produced) was affected by alien HP receipt and whether the effect varied between native and alien recipients. HP transfer networks exhibit relatively high connectance (c. 15%), suggesting high HP transfer within the studied communities. Significant network nestedness further suggests the existence of species that predominantly act as HP donors or recipients in the community. Species-level analyses showed that natives receive 80% more HP compared to alien species, and that alien plants donate 40% more HP than natives. HP receipt and donation were mediated by different floral traits and such effects were independent of plant origin (native or alien). The proportion of alien HP received significantly affected conspecific pollen tube success in natives, but not that of alien species. Synthesis. Our results suggest that HP transfer in invaded communities is widespread, and that native and alien species play different roles within HP transfer networks, which are mediated by a different suite of floral traits. Alien species, in particular, play a central role as HP donors and are more tolerant to HP receipt than natives—a finding that points to two overlooked mechanisms facilitating alien plant invasion and success within native co-flowering communities.

Flower phenotype may diverge within plant lineages when moving across “pollinator climates” (geographic differences in pollinator abundance or preference). Here we explored the potential importance of pollinators as drivers of floral color diversification in the nightshade genus Jaborosa, taking into account color perception capabilities of the actual pollinators (nocturnal hawkmoths vs. saprophilous flies) under a geographic perspective. We analyzed the association between transitions across environments and perceptual color axes using comparative methods. Our results revealed two major evolutionary themes in Jaborosa: (1) a “warm subtropical sphingophilous clade” composed of three hawkmoth-pollinated species found in humid lowland habitats, with large white flowers that clustered together in the visual space of a model hawkmoth (Manduca sexta) and a “cool-temperate brood-deceptive clade” composed of largely fly-pollinated species with small dark flowers found at high altitudes (Andes) or latitudes (Patagonian Steppe), that clustered together in the visual space of a model blowfly (Lucilia sp.) and a syrphid fly (Eristalis tenax). Our findings suggest that the ability of plants to colonize newly formed environments during Andean orogeny and the ecological changes that followed were concomitant with transitions in flower color as perceived by different pollinator functional groups. Our findings suggest that habitat and pollination mode are inextricably linked in the history of this South American plant lineage. Fil: Moré, Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Ibañez, Ana Clara. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Drewniak, María Eugenia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Cocucci, Andrea Aristides. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Raguso, Robert A.. Cornell University; Estados Unidos

A challenge for chemical ecologists is to understand the ecological functions of complex essential oils (EOs) produced by plants. Sensitive analytical methods, genetic manipulation/plant breeding, and sophisticated physiological/behavioral bioassays have facilitated progress toward this goal. Aromatic plants from Mediterranean environments are important natural sources of essential oils. Multidisciplinary studies revealed fine-scale geographic polymorphism in foliar EOs from Thymus vulgaris in southern France. Single monoterpenoids dominate these “chemotypes,” whose adaptive value depends on soil type, local climate, herbivore pressure, and competition with neighboring plants. Similar habitats in Greece feature aromatic shrubs (Cistus creticus, Lavandula stoechas) that serve as hubs in plant-pollinator networks dominated by native bees. The putative connection between sesquiterpene EOs and non-volatile resins, collected from these plants by bees as propolis, is reminiscent of well-documented resin collection in tropical habitats, from specialized Dalechampia and Clusia flowers as well as wounded trees, to be used as nesting materials by female stingless bees and orchid bees. In the same habitats, male orchid bees collect EOs from hundreds of orchid species along with Anthurium species in the Araceae family, providing specialized pollination services. The chapter closes with a survey of rewarding and deceptive pollination modes driven by EO chemistry in the aroid family.

Experimental investigations of the ecological importance of floral scent are increasingly performed in the context of other floral traits, such as color, shape and orientation. Such studies typically adopt one of three experimental approaches to manipulate floral scent: floral augmentation (adding scent to a flower), floral deconstruction (decoupling scent and other traits of living flowers) or floral reconstruction (recombining scent with other traits, using artificial flowers or flower parts). Such approaches have established the importance of multi-modal sensory attraction across the full spectrum of generalized to specialized pollination systems. This chapter outlines the multitude of ways that floral scent interacts with other floral traits, under different ecological contexts, with reference to a growing body of theory concerning how biotic and abiotic factors influence floral display. It is now clear that scent interacts with other floral traits to influence plant–pollinator network structure, reproductive isolation, host specialization, obligate mutualism, evolutionary pollinator shifts, floral mimicry, sexual and brood-site deception.

A current frontier of character displacement research is to determine if displacement occurs via multiple phenotypic pathways and varies across communities with different species compositions. Here, we conducted the first test for context-dependent character displacement in multimodal floral signals by analyzing variation in floral scent in a system that exhibits character displacement in flower size, and that has multiple types of sympatric communities. In a greenhouse common garden experiment, we measured quantitative variation in volatile emission rates of the progeny of two species ofClarkiafrom replicated communities that contain one, two, or fourClarkiaspecies. The first two axes of a constrained correspondence analysis, which explained 24 percent of the total variation in floral scent, separated the species and community types, respectively. Of the 23 compounds that were significantly correlated with these axes, nine showed patterns consistent with character displacement. Two compounds produced primarily byC. unguiculataand two compounds produced primarily byC. cylindricawere emitted in higher amounts in sympatry. Character displacement in some volatiles varied across sympatric communities and occurred in parallel with displacement in flower size, demonstrating that this evolutionary process can be context-dependent and may occur through multiple pathways.

The hydrocarbon pattern in the floral scent of Yucca species was found to comprise a group of unbranched, mid-chain alkanes, alkenes, and an alkadiene. In Y. reverchonii, highly dominant (Z)-8-heptadecene is accompanied by (6Z,9Z)-6,9-heptadecadiene and heptadecane as minor components and by traces of other saturated and unsaturated hydrocarbons with similar chain length. Some of these volatiles proved to be perceived by the antennae of Tegeticula cassandra (pollinating seed-eater of Yucca) and Prodoxus decipiens (herbivore on Yucca). The possible biosynthesis of the compounds is discussed.

Premise of research. Jackfruit (Artocarpus heterophyllus, Moraceae) is an emerging but underutilized crop whose pollination is poorly understood. We present a multidisciplinary investigation of the...

Angiosperm flowers have evolved a dazzling palette of colours and a rich bouquet of scents, principally serving to attract pollinators. Despite recent progress in the ecology of pollination, the sensory floral traits that are important for communication with pollinators (for example, colour and scent) have not been assessed in an unbiased, integrative sense within a community context. Nonetheless, floral sensory stimuli are known key factors that mediate flower visitation, thus affecting community dynamics. Here we show that flowers of the phrygana, a natural Mediterranean scrubland, display integrated patterns of scent composition and colour (as perceived by pollinators). Surprisingly, the data reveal predictive relationships between patterns of volatile composition and flower reflectance spectra. The presence of nectar is related to visual cues and the qualitative composition of floral aromas. Our results reveal a coordinated phenotypic integration consistent with the sensory abilities and perceptual biases of bees, suggesting potential facilitative effects for pollination and highlighting the fundamental importance of bees in Mediterranean-type ecosystems. We offer our unbiased approach as a starting point for more extensive, global investigations of the diversity of floral sensory phenotypes and its role in the community ecology of plant-pollinator interactions.

Premise of research. Tacca is a monocot genus characterized by an unusual reproductive display, with plants possessing umbelliform inflorescences subtended by highly conspicuous leafy bracts and filiform bracteoles with colors ranging from dark maroon to white. Paradoxically, previous studies indicated very low levels of outcrossing in some showy Tacca species, implicating self-pollination as the primary reproductive strategy.Methodology. We describe visual observations and collections made of floral visitors to flowering individuals of Tacca cristata Jack in Singapore.Pivotal results. Female ceratopogonid midges were observed to visit the flowers at anthesis and were collected with pollen specifically placed on their dorsal thoracic region. A significant proportion of flowering plants was attacked by florivores.Conclusions. These findings suggest that at least some showy species of Tacca may be pollinated to some extent through insect visitation. The reproductive biology of Tacca, including inflorescence...

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta‐analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals., The project was supported by the Graduate School ‘Evolutionary Networks: Organisms, Reactions, Molecules’ (E‐Norm) of the Heinrich‐Heine‐University, Düsseldorf, Germany, the Max Planck Society and the Deutsche Forschungsgemeinschaft (DFG JU 2856/1‐1 and DFG JU 2856/2‐2).

Floral scents can act as important contributing factors to plant reproductive isolation mediated by pollinators. Plants may utilize fetid floral odors that specifically lure saprophilous flies seeking high protein content substrates, such as dung or carrion, to reach sexual maturity or as food sources for their larvae. In this work, we used baits with fetid volatile organic compounds (VOCs) that are produced during the decay of animal protein substrates (oligosulfides and a fermented bone-meal blend) to evaluate the role that olfactory signals may have played in the shift to saprophilous fly pollination in species of the nightshade genus Jaborosa Juss. Traps with the fetid baits attracted the same assemblage of saprophilous fly species that were recorded pollinating the flowers in different populations of the Andean-distributed species J. laciniata, whereas no flies were attracted to the control traps using mineral oil. Furthermore, the addition of oligosulfides to flowers of J. integrifolia, a lowland distributed species pollinated by nocturnal hawkmoths, resulted in the nearly immediate attraction of saprophilous flies (mainly Calliphoridae) to the flowers. These results provide evidence that the emission of fetid floral VOCs is sufficient to attract flies to flowers irrespective of other flower features and geographic region. This suggests that the evolutionary shift to saprophilous fly pollination in the genus Jaborosa could have been initiated with novel floral visitors attracted by the emission of fetid VOCs and then followed by major changes in other flower traits such as corolla color and morphology to optimize pollen export and placement. Fil: Moré, Marcela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba; Argentina Fil: Mulieri, Pablo Ricardo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”; Argentina Fil: Battan Horenstein, Moira. Universidad Nacional de Córdoba; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto de Diversidad y Ecología Animal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto de Diversidad y Ecología Animal; Argentina Fil: Cocucci, Andrea Aristides. Universidad Nacional de Córdoba; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina Fil: Raguso, Robert A.. Cornell University; Estados Unidos

Solitary insects that feed on floral nectar must use innate knowledge to find their first flower. While innate preferences for flower colours are often described as fixed, species-specific traits, the nature and persistence of these preferences have been debated, particularly in relation to ontogenetic processes such as learning. Here we present evidence for a strong context-dependence of innate colour preferences in the crepuscular hawkmothManduca sexta. Contrary to expectations, our results show that innate colour biases shift with changes in the visual environment, namely illuminance and background. This finding reveals that innate responses might emerge from a contextual integration of sensory inputs involved in object class recognition rather than from the deterministic matching of such inputs with a fixed internal representation.

A major challenge in evolutionary biology is to understand how complex traits of multiple functions have diversified and codiversified across interacting lineages and geographic ranges. We evaluate intra- and interspecific variation in floral scent, which is a complex trait of documented importance for mutualistic and antagonistic interactions between plants, pollinators, and herbivores. We performed a large-scale, phylogenetically structured study of an entire plant genus (Lithophragma, Saxifragaceae), of which several species are coevolving with specialized pollinating floral parasites of the moth genus Greya (Prodoxidae). We sampled 94 Lithophragma populations distributed across all 12 recognized Lithophragma species and subspecies, and four populations of related saxifragaceous species. Our results reveal an unusually high diversity of floral volatiles among populations, species, and clades within the genus. Moreover, we found unexpectedly major changes at each of these levels in the biosynthetic pathways used by local populations in their floral scents. Finally, we detected significant, but variable, genus- and species-level patterns of ecological convergence in the floral scent signal, including an impact of the presence and absence of two pollinating Greya moth species. We propose that one potential key to understanding floral scent variation in this hypervariable genus is its geographically diverse interactions with the obligate specialized Greya moths and, in some species and sites, more generalized copollinators.

Trichogramma ostriniae is a parasitoid wasp species that is used as a biological control for several lepidopteran agricultural pests. Our study examined the effects of relative humidity (RH) on the behaviour of female T. ostriniae. In Y-tube RH choice assays, wasps generally chose higher RH over lower RH but the latency time taken to make a choice displayed no clear patterns that could be ascribed to the magnitude of the RH difference between arms of the Y-tube. In trials conducted in glass arenas with fixed humidities, the conditional probabilities of transition from searching to interacting with the leaf disk, and from interacting with leaf disks to antennal egg drumming and oviposition, were not significantly different among the RH levels, nor were there differences in latency times. These findings suggest that the level of RH may influence habitat choice but have little effect on search efficacy.

All plants synthesize a suite of several hundred terpenoid compounds with roles that include phytohormones, protein modification reagents, anti-oxidants, and more. Different plant lineages also synthesize hundreds of distinct terpenoids, with the total number of such specialized plant terpenoids estimated in the scores of thousands. Phylogenetically restricted terpenoids are implicated in defense or in the attraction of beneficial organisms. A popular hypothesis is that the ability of plants to synthesize new compounds arose incrementally by selection when, as a result of gradual changes in their biotic partners and enemies, the 'old' plant compounds were no longer effective, a process dubbed the 'coevolutionary arms race'. Another hypothesis posits that often the sheer diversity of such compounds provides benefits that a single compound cannot. In this article, we review the unique features of the biosynthetic apparatus of terpenes in plants that facilitate the production of large numbers of distinct terpenoids in each species and how facile genetic and biochemical changes can lead to the further diversification of terpenoids. We then discuss evidence relating to the hypotheses that given ecological functions may be enhanced by the presence of mixtures of terpenes and that the acquisition of new functions by terpenoids may favor their retention once the original functions are lost.