RESUMEN
The ecological interaction between fleshy fruits and frugivores is influenced by diverse mixtures of secondary metabolites that naturally occur in the fruit pulp. Although some fruit secondary metabolites have a primary role in defending the pulp against antagonistic frugivores, these metabolites also potentially affect mutualistic interactions. The physiological impact of these secondary metabolites on mutualistic frugivores remains largely unexplored. Using a mutualistic fruit bat (Carollia perspicillata), we showed that ingesting four secondary metabolites commonly found in plant tissues affects bat foraging behavior and induces changes in the fecal metabolome. Our behavioral trials showed that the metabolites tested typically deter bats. Our metabolomic surveys suggest that secondary metabolites alter, either by increasing or decreasing, the absorption of essential macronutrients. These behavioral and physiological effects vary based on the specific identity and concentration of the metabolite tested. Our results also suggest that a portion of the secondary metabolites consumed is excreted by the bat intact or slightly modified. By identifying key shifts in the fecal metabolome of a mutualistic frugivore caused by secondary metabolite consumption, this study improves our understanding of the effects of fruit chemistry on frugivore physiology.
RESUMEN
Ripe fleshy fruits contain not only nutrients but also a diverse array of secondary metabolites. Nutrients serve as a reward for mutualists, whereas defensive metabolites protect the fruit against pests and predators. The composition of these chemical traits is highly variable, both across different plants and even within repeating structures on the same individual plant. This intraspecific and intraindividual variation has important fitness consequences for both plants and animals, yet patterns of variation and covariation in nutrients and secondary metabolites are not well understood, especially at smaller scales. Here, we investigate the multiscale variation and covariation between nutrients and defensive metabolites in Piper sancti-felicis ripe fruits. Means and measures of variation of sugars, proteins, phenolics, and alkenylphenols vary greatly among plants, and at least 50% of the trait variation occurs at the intraindividual level. Also, we found that proteins, but not sugars, were correlated with phenolics and alkenylphenols at multiple scales, suggesting trait variation in protein content may be more constrained than sugars. Our findings emphasize the importance of examining patterns across scales and provide the groundwork to better understand how complex patterns of variation and covariation in nutrients and defensive metabolites shape ecological interactions surrounding fruits.
RESUMEN
Plant secondary metabolites are key mechanistic drivers of species interactions. These metabolites have primarily been studied for their role in defense, but they can also have important consequences for mutualisms, including seed dispersal. Although the primary function of fleshy fruits is to attract seed-dispersing animals, fruits often contain complex mixtures of toxic or deterrent secondary metabolites that can reduce the quantity or quality of seed dispersal mutualisms. Furthermore, because seeds are often dispersed across multiple stages by several dispersers, the net consequences of fruit secondary metabolites for the effectiveness of seed dispersal and ultimately plant fitness are poorly understood. Here, we tested the effects of amides, nitrogen-based defensive compounds common in fruits of the neotropical plant genus Piper (Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts to Piper fruits both in the field and lab, finding that amides reduced the quantity of secondary seed dispersal by reducing ant recruitment (87%) and fruit removal rates (58% and 66% in the field and lab, respectively). Moreover, amides not only reduced dispersal quantity but also altered seed dispersal quality by shifting the community composition of recruiting ants (notably by reducing the recruitment of the most effective disperser by 90% but having no detectable effect on the recruitment of a cheater species that removes fruit pulp without dispersing seeds). Although amides did not affect the distance ants initially carried seeds, they altered the quality of seed dispersal by reducing the likelihood of ants cleaning seeds (67%) and increasing their likelihood of ants redispersing seeds outside of the nest (200%). Overall, these results demonstrate that secondary metabolites can alter the effectiveness of plant mutualisms, by both reducing mutualism quantity and altering mutualism quality through multiple mechanisms. These findings present a critical step in understanding the factors mediating the outcomes of seed dispersal and, more broadly, demonstrate the importance of considering how defensive secondary metabolites influence the outcomes of mutualisms surrounding plants.
Asunto(s)
Hormigas , Dispersión de Semillas , Animales , Frutas , Simbiosis , SemillasRESUMEN
Microbial communities associated with fruit can contribute to quality and pathogen resistance, but little is known about their assembly and dynamics during fruit development and storage. Three apple cultivars growing under the same environmental conditions were utilized to examine the apple carposphere microbiome composition and structure at different developmental stages and storage. There was a significant effect (Adonis, p ≤ 0.001) of fruit genotype and its developmental stages and storage times on the fruit surface microbial assemblage and a strong temporal microbial community succession was detected (Mantel test: R ≤ 0.5, p = 0.001) in both bacterial and fungal communities. A set of 15 bacterial and 35 fungal core successional taxa and members exhibiting differential abundances at different fruit stages were identified. For the first time, we show the existence of underlying universal dynamics in the assembly of fruit-associated microbiomes. We also provide evidence of strong microbial cross-domain associations and uncover potential microbe-microbe correlations in the apple carposphere. Together our findings shed light on how the fruit carposphere assemble and change over time, and provide new insights into fruit microbial ecology.
RESUMEN
Interactions between plants and leaf herbivores have long been implicated as the major driver of plant secondary metabolite diversity. However, other plant-animal interactions, such as those between fruits and frugivores, may also be involved in phytochemical diversification. Using 12 species of Piper, we conducted untargeted metabolomics and molecular networking with extracts of fruits and leaves. We evaluated organ-specific secondary metabolite composition and compared multiple dimensions of phytochemical diversity across organs, including richness, structural complexity, and variability across samples at multiple scales within and across species. Plant organ identity, species identity, and the interaction between the two all significantly influenced secondary metabolite composition. Leaves and fruit shared a majority of compounds, but fruits contained more unique compounds and had higher total estimated chemical richness. While the relative levels of chemical richness and structural complexity across organs varied substantially across species, fruit diversity exceeded leaf diversity in more species than the reverse. Furthermore, the variance in chemical composition across samples was higher for fruits than leaves. By documenting a broad pattern of high phytochemical diversity in fruits relative to leaves, this study lays groundwork for incorporating fruit into a comprehensive and integrative understanding of the ecological and evolutionary factors shaping secondary metabolite composition at the whole-plant level.
RESUMEN
Plant secondary metabolites (PSMs) play a central role in seed dispersal and fruit defense, with potential for large impacts on plant fitness and demography. Yet because PSMs can have multiple interactive functions across seed dispersal stages, we must systematically study their effects to determine the net consequences for plant fitness. To tackle this issue, we integrate the role of fruit PSMs into the seed dispersal effectiveness (SDE) framework. We describe PSM effects on the quantity and quality of animal-mediated seed dispersal, both in pairwise interactions and diverse disperser communities, as well as trade-offs that occur across dispersal stages. By doing so, this review provides structure to a rapidly growing field and yields insights into a critical process shaping plant populations.
Asunto(s)
Dispersión de Semillas , Animales , Frutas , SemillasRESUMEN
The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested a set of predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer-specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.
Asunto(s)
Biodiversidad , Plantas , Evolución Biológica , FitoquímicosRESUMEN
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
RESUMEN
Deciphering the ecological roles of plant secondary metabolites requires integrative studies that assess both the allocation patterns of compounds and their bioactivity in ecological interactions. Secondary metabolites have been primarily studied in leaves, but many are unique to fruits and can have numerous potential roles in interactions with both mutualists (seed dispersers) and antagonists (pathogens and predators). We described 10 alkenylphenol compounds from the plant species Piper sancti-felicis (Piperaceae), quantified their patterns of intraplant allocation across tissues and fruit development, and examined their ecological role in fruit interactions. We found that unripe and ripe fruit pulp had the highest concentrations and diversity of alkenylphenols, followed by flowers; leaves and seeds had only a few compounds at detectable concentrations. We observed a nonlinear pattern of alkenylphenol allocation across fruit development, increasing as flowers developed into unripe pulp then decreasing as pulp ripened. This pattern is consistent with the hypothesis that alkenylphenols function to defend fruits from pre-dispersal antagonists and are allocated based on the contribution of the tissue to the plant's fitness, but could also be explained by non-adaptive constraints. To assess the impacts of alkenylphenols in interactions with antagonists and mutualists, we performed fungal bioassays, field observations, and vertebrate feeding experiments. In fungal bioassays, we found that alkenylphenols had a negative effect on the growth of most fungal taxa. In field observations, nocturnal dispersers (bats) removed the majority of infructescences, and diurnal dispersers (birds) removed a larger proportion of unripe infructescences. In feeding experiments, bats exhibited an aversion to alkenylphenols, but birds did not. This observed behavior in bats, combined with our results showing a decrease in alkenylphenols during ripening, suggests that alkenylphenols in fruits represent a trade-off (defending against pathogens but reducing disperser preference). These results provide insight into the ecological significance of a little studied class of secondary metabolites in seed dispersal and fruit defense. More generally, documenting intraplant spatiotemporal allocation patterns in angiosperms and examining mechanisms behind these patterns with ecological experiments is likely to further our understanding of the evolutionary ecology of plant chemical traits.
Asunto(s)
Frutas , Dispersión de Semillas , Animales , Aves , Hojas de la Planta , SemillasRESUMEN
Poison ivy (Toxicodendron radicans) is best known for causing exasperating allergenic delayed-contact dermatitis symptoms that last for weeks on persons who have contacted the plant. Urushiols are alkylcatechols produced by poison ivy responsible for causing this dermatitis. While urushiol chemical structures are well known, the metabolic intermediates and genes responsible for their biosynthesis have not been experimentally validated. A molecular genetic characterization of urushiol biosynthesis in poison ivy will require stable genetic transformation and subsequent regeneration of organs that retain the capacity synthesize urushiol. To this end, Agrobacterium rhizogenes was used to generate hormone-independent poison ivy hairy root cultures. Optimal conditions for hairy root formation were skotomorphic poison ivy hypocotyls prick-inoculated with A. rhizogenes, and preferential propagation of cultures with an atypical clumpy hairy root growth habit. The origin of the poison ivy accession used for A. rhizogenes prick-inoculation did not affect the initial formation of calli/hairy root primordia, but rather significantly influenced the establishment of long-term hormone-independent hairy root growth. A. rhizogenes harboring a recombinant T-DNA binary plasmid with an intron-containing Firefly Luciferase gene produced stable transgenic hairy root lines expressing luciferase activity at high frequency. Poison ivy hairy root lines produced significantly lower steady-state urushiol levels relative to wild-type roots, but higher urushiol levels than a poison ivy undifferentiated callus line with undetectable urushiol levels, suggesting that urushiol biosynthesis requires intact poison ivy organs. The lower urushiol levels in poison ivy hairy root lines facilitated the first identification of anacardic acid metabolites initially in hairy roots, and subsequently in wild-type roots as well. This study establishes a transformation hairy root regeneration protocol for poison ivy that can serve as a platform for future reverse-genetic studies of urushiol biosynthesis in poison ivy hairy roots.
RESUMEN
There is growing recognition of the role that the microbiome plays in the health and physiology of many plant species. However, considerably less research has been conducted on the postharvest microbiome of produce and the impact that postharvest processing may have on its composition. Here, amplicon sequencing was used to study the effect of washing, waxing, and low-temperature storage at 2 °C for six months on the bacterial and fungal communities of apple calyx-end, stem-end, and peel tissues. The results of the present work reveal that tissue-type is the main factor defining fungal and bacterial diversity and community composition on apple fruit. Both postharvest treatments and low temperature storage had a strong impact on the fungal and bacterial diversity and community composition of these tissue types. Distinct spatial and temporal changes in the composition and diversity of the microbiota were observed in response to various postharvest management practices. The greatest impact was attributed to sanitation practices with major differences among unwashed, washed and washed-waxed apples. The magnitude of the differences, however, was tissue-specific, with the greatest impact occurring on peel tissues. Temporally, the largest shift occurred during the first two months of low-temperature storage, although fungi were more affected by storage time than bacteria. In general, fungi and bacteria were impacted equally by sanitation practices, especially the epiphytic microflora of peel tissues. This research provides a foundation for understanding the impact of postharvest management practices on the microbiome of apple and its potential subsequent effects on postharvest disease management and food safety.
RESUMEN
Carrot (Daucus carota L.) is an important root vegetable crop with high nutritional value, characteristic flavor, and benefits to human health. D. carota tissues produce an essential oil that is rich in volatile terpenes and plays a major role in carrot aroma and flavor. Although terpene composition represents a critical quality attribute of carrots, little is known about the biosynthesis of terpenes in this crop. Here, we functionally characterized 19 terpene synthase (TPS) genes in an orange carrot (genotype DH1) and compared tissue-specific expression profiles and in vitro products of their recombinant proteins with volatile terpene profiles from DH1 and four other colored carrot genotypes. In addition to the previously reported (E)-ß-caryophyllene synthase (DcTPS01), we biochemically characterized several TPS proteins with direct correlations to major compounds of carrot flavor and aroma including germacrene D (DcTPS7/11), γ-terpinene (DcTPS30) and α-terpinolene (DcTPS03). Random forest analysis of volatiles from colored carrot cultivars identified nine terpenes that were clearly distinct among the cultivars and likely contribute to differences in sensory quality. Correlation of TPS gene expression and terpene metabolite profiles supported the function of DcTPS01 and DcTPS03 in these cultivars. Our findings provide a roadmap for future breeding efforts to enhance carrot flavor and aroma.
Asunto(s)
Transferasas Alquil y Aril/genética , Regulación de la Expresión Génica de las Plantas , Proteínas de Plantas/genética , Terpenos/metabolismo , Daucus carota , Odorantes , Aceites Volátiles/metabolismoRESUMEN
Morphological and chemical attributes of diaspores in myrmecochorous plants have been shown to affect seed dispersal by ants, but the relative importance of these attributes in determining seed attractiveness and dispersal success is poorly understood. We explored whether differences in diaspore morphology, elaiosome fatty acids, or elaiosome phytochemical profiles explain the differential attractiveness of five species in the genus Trillium to eastern North American forest ants. Species were ranked from least to most attractive based on empirically-derived seed dispersal probabilities in our study system, and we compared diaspore traits to test our hypotheses that more attractive species will have larger diaspores, greater concentrations of elaiosome fatty acids, and distinct elaiosome phytochemistry compared to the less attractive species. Diaspore length, width, mass, and elaiosome length were significantly greater in the more attractive species. Using gas chromatography-mass spectrometry, we found significantly higher concentrations of oleic, linoleic, hexadecenoic, stearic, palmitoleic, and total fatty acids in elaiosomes of the more attractive species. Multivariate assessments revealed that elaiosome phytochemical profiles, identified through liquid chromatography-mass spectrometry, were more homogeneous for the more attractive species. Random forest classification models (RFCM) identified several elaiosome phytochemicals that differed significantly among species. Random forest regression models revealed that some of the compounds identified by RFCM, including methylhistidine (α-amino acid) and d-glucarate (carbohydrate), were positively related to seed dispersal probabilities, while others, including salicylate (salicylic acid) and citrulline (L-α-amino acid), were negatively related. These results supported our hypotheses that the more attractive species of Trillium-which are geographically widespread compared to their less attractive, endemic congeners-are characterized by larger diaspores, greater concentrations of fatty acids, and distinct elaiosome phytochemistry. Further advances in our understanding of seed dispersal effectiveness in myrmecochorous systems will benefit from a portrayal of dispersal unit chemical and physical traits, and their combined responses to selection pressures.
RESUMEN
Research on the ecological and evolutionary roles of phytochemicals has recently progressed from studying single compounds to examining chemical diversity itself. A key conceptual advance enabling this progression is the use of species diversity metrics for quantifying phytochemical diversity. In this perspective, we extend the theory developed for species diversity to further our understanding of what exactly phytochemical diversity is and how its many dimensions impact ecological and evolutionary processes. First, we discuss the major dimensions of phytochemical diversity - richness, evenness, functional diversity, and alpha, gamma and beta diversity. We describe their potential independent roles in biotic interactions and the practical challenges associated with their analysis. Second, we re-analyse the published and unpublished datasets to reveal that the phytochemical diversity experienced by an organism (or observed by a researcher) depends strongly on the scale of the interaction and the total amount of phytochemicals involved. We argue that we must account for these frames of reference to meaningfully understand diversity. Moving from a general notion of phytochemical diversity as a single measure to a precise definition of its multidimensional and multiscale nature yields overlooked testable predictions that will facilitate novel insights about the evolutionary ecology of plant biotic interactions.
Asunto(s)
Biodiversidad , Fitoquímicos , Evolución Biológica , EcologíaRESUMEN
The paradoxical presence of toxic chemical compounds in ripe fruits represents a balance between plant enemies and allies: chemical traits can defend seeds against antagonistic herbivores, seed predators, or fungal pathogens, but also can impose costs by repelling mutualistic seed dispersers, although the costs are often difficult to quantify. Seeds gain fitness benefits from traveling far from the parent plant, as they can escape from parental competition and elude specialized herbivores as well as pathogens that accumulate on adult plants. However, seeds are difficult to follow from their parent plant to their final destination. Thus, little is known about the factors that determine seed dispersal distance. We investigated this potential cost of fruit secondary compounds, reduced seed dispersal distance, by combining two data sets from previous work on a Neotropical bat-plant dispersal system (bats in the genus Carollia and plants in the genus Piper). We used data from captive behavioral experiments, which show how amides in ripe fruits of Piper decrease the retention time of seeds and alter food choices. With new analyses, we show that these defensive secondary compounds also delay the time of fruit removal. Next, with a behaviorally annotated bat telemetry data set, we quantified post-feeding movements (i.e., seed dispersal distances). Using generalized additive mixed models we found that seed dispersal distances varied nonlinearly with gut retention times as well as with the time of fruit removal. By interrogating the model predictions, we identified two novel mechanisms by which fruit secondary compounds can impose costs in terms of decreased seed dispersal distances: (1) small-scale reductions in gut retention time and (2) causing fruits to forgo advantageous bat activity peaks that confer high seed dispersal distances.
Asunto(s)
Quirópteros , Dispersión de Semillas , Animales , Conducta Alimentaria , Frutas , Herbivoria , SemillasRESUMEN
BACKGROUND AND AIMS: Most crops have been dramatically altered from their wild ancestors with the primary goal of increasing harvestable yield. A long-held hypothesis is that increased allocation to yield has reduced plant investment in defence and resulted in crops that are highly susceptible to pests. However, clear demonstrations of these trade-offs have been elusive due to the many selective pressures that occur concurrently during crop domestication. METHODS: To provide a robust test of whether increased allocation to yield can alter plant investment in defence, this study examined fruit chemical defence traits and herbivore resistance across 52 wild and 56 domesticated genotypes of apples that vary >26-fold in fruit size. Ninety-six phenolic metabolites were quantified in apple skin, pulp and seeds, and resistance to the codling moth was assessed with a series of bioassays. KEY RESULTS: The results show that wild apples have higher total phenolic concentrations and a higher diversity of metabolites than domesticated apples in skin, pulp and seeds. A negative phenotypic relationship between fruit size and phenolics indicates that this pattern is driven in part by allocation-based trade-offs between yield and defence. There were no clear differences in codling moth performance between wild and domesticated apples and no overall effects of total phenolic concentration on codling moth performance, but the results did show that codling moth resistance was increased in apples with higher phenolic diversity. The concentrations of a few individual compounds (primarily flavan-3-ols) also correlated with increased resistance, primarily driven by a reduction in pupal mass of female moths. CONCLUSIONS: The negative phenotypic relationship between fruit size and phenolic content, observed across a large number of wild and domesticated genotypes, supports the hypothesis of yield-defence trade-offs in crops. However, the limited effects of phenolics on codling moth highlight the complexity of consequences that domestication has for plant-herbivore interactions. Continued studies of crop domestication can further our understanding of the multiple trade-offs involved in plant defence, while simultaneously leading to novel discoveries that can improve the sustainability of crop production.
Asunto(s)
Malus , Mariposas Nocturnas , Animales , Domesticación , Femenino , Frutas , Asignación de RecursosRESUMEN
Plant responses induced by herbivore damage can provide fitness benefits, but can also have important costs due to altered interactions with mutualist pollinators. We examined the effects of plant responses to herbivory in a hummingbird-pollinated distylous shrub, Palicourea angustifolia. Through a series of field experiments we investigated whether damage from foliar herbivores leads to a reduction in fruit set, influences floral visitation, or alters floral traits that may influence pollinator preference or pollinator efficiency. Foliar herbivory by a generalist grasshopper led to reduced fruit set in branches that were directly damaged as well as in adjacent undamaged branches on the same plant. Furthermore, herbivory resulted in reduced floral visitation from two common hummingbird species and two bee species. An investigation into the potential mechanisms behind reduced floral visitation in induced plants showed that foliar herbivore damage resulted in shorter styles and lower nectar volumes. This reduction in style length could reduce pollen deposition between different floral morphs that is required for optimal pollination in a distylous plant. We did not detect any differences in the volatile blends released by damaged and undamaged branches, suggesting that foliar herbivore-induced changes in floral morphology and rewards, and not volatile blends, are the primary mechanism mediating changes in visitation. Our results provide novel mechanisms for how plant responses induced by foliar herbivores can lead to ecological costs.
Asunto(s)
Aves/fisiología , Herbivoria , Insectos/fisiología , Hojas de la Planta/fisiología , Polinización , Animales , Flores/fisiología , VolatilizaciónRESUMEN
For millennia, humans have imposed strong selection on domesticated crops, resulting in drastically altered crop phenotypes compared with wild ancestors. Crop yields have increased, but a long-held hypothesis is that domestication has also unintentionally decreased plant defences against herbivores. To test this hypothesis, we conducted a phylogenetically controlled meta-analysis comparing insect herbivore resistance and putative plant defence traits between crops and their wild relatives. Our database included 2098 comparisons made across 73 crops in 89 studies. We found that domestication consistently reduced plant resistance to herbivores, although the magnitude of the effects varied across plant organs and depended on how resistance was measured. However, domestication had no consistent effects on the specific plant defence traits underlying resistance, including secondary metabolites and physical feeding barriers. The values of these traits sometimes increased and sometimes decreased during domestication. Consistent negative effects of domestication were observed only when defence traits were measured in reproductive organs or in the plant organ that was harvested. These results highlight the complexity of evolution under domestication and the need for an improved theoretical understanding of the mechanisms through which agronomic selection can influence the species interactions that impact both the yield and sustainability of our food systems.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.
Asunto(s)
Antibiosis , Evolución Biológica , Productos Agrícolas/fisiología , Domesticación , Herbivoria , Insectos/fisiología , Animales , Cadena AlimentariaRESUMEN
Agriculture is a dominant evolutionary force that drives the evolution of both domesticated and wild species. However, the various mechanisms of agriculture-induced evolution and their socio-ecological consequences are not often synthetically discussed. Here, we explore how agricultural practices and evolutionary changes in domesticated species cause evolution in wild species. We do so by examining three processes by which agriculture drives evolution. First, differences in the traits of domesticated species, compared with their wild ancestors, alter the selective environment and create opportunities for wild species to specialize. Second, selection caused by agricultural practices, including both those meant to maximize productivity and those meant to control pest species, can lead to pest adaptation. Third, agriculture can cause non-selective changes in patterns of gene flow in wild species. We review evidence for these processes and then discuss their ecological and sociological impacts. We finish by identifying important knowledge gaps and future directions related to the eco-evolutionary impacts of agriculture including their extent, how to prevent the detrimental evolution of wild species, and finally, how to use evolution to minimize the ecological impacts of agriculture.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.