Plant-pollinator Associations Research Articles

Soil–Plant–Pollinator Relationships in Urban Grass and Meadow Habitats: Competing Benefits and Demands of Tall Flowering Plants on Soil and Pollinator Diversity

Urban green spaces can be important habitats for soil, plant, and pollinator diversity and the complementary ecosystem functions they confer. Most studies tend to investigate the relationships between plant diversity with either soil or pollinator diversity, but establishing their relationship across habitat types could be important for optimising ecosystem service provision via alternative management (for instance, urban meadows in place of short amenity grass). Here, we investigate soil–plant–pollinator relationships across urban grass and meadow habitats through a range of measured biodiversity (soil mesofauna and macrofauna, plants, aboveground invertebrates, and pollinators) and edaphic variables. We found significant effects of habitat type on available nutrients (plant and soil C:N ratios) but less clear relationships were observed between habitat type and diversity metrics. Soil–plant–pollinator interactions across habitat types and sites showed an interconnection, whereby flowering plant abundance increased alongside soil macrofauna abundance. Site characteristics that showed strong effects on plant and invertebrate diversity metrics were C:N ratios (plant and soil) and soil pH, suggesting a potential role of nutrient availability on soil–plant–pollinator associations. Our results suggest that a combination of short-mown grass, tall grass, and sown flowers can provide greater benefits for soil and pollination services as each habitat type benefits different taxa due to differing sensitivities to management practices. For example, pollinators benefit from sown flowers but soil fauna are sensitive to annual sowing. Our results also indicate that sown flowers may not optimise overall biodiversity as expected due to disturbance and the depleting role of tall, flowering plants on soil nutrient availability. Future research across a greater range of sites in urban landscapes would resolve the potential role of nutrient availability in modulating soil–plant–pollinator interactions in urban green spaces.

Fields of flowers with few strikes: how oligolectic bees manage their foraging behavior on Calibrachoa elegans (Solanaceae).

In specialized plant-pollinator associations, partners may exhibit adaptive traits, which favor the maintenance of the interaction. The association between Calibrachoa elegans (Solanaceae) and its oligolectic bee pollinator, Hexantheda missionica (Colletidae), is mutualistic and forms a narrowly specialized pollination system. Flowers of C. elegans are pollinated exclusively by this bee species, and the bees restrict their pollen resources to this plant species. The pollen presentation schedules of C. elegans were evaluated at the population level to test the hypothesis that H. missionica females adjust their foraging behavior to the resource offering regime of C. elegans plants. For this, the number of new flowers and anthers opened per hour (as a proxy for pollen offering) was determined, and pollen advertisement was correlated with the frequency of flower visits during the day. Preferences of female bees for flowers of different stages were also investigated, and their efficiency as pollinators was evaluated. Pollen offering by C. elegans was found to be partitioned throughout the day through scattered flower openings. Females of H. missionica indeed adjusted their foraging activity to the most profitable periods of pollen availability. The females preferred new, pollen-rich flowers over old ones and gathered pollen and nectar selectively according to flower age. Such behaviors must optimize female bee foraging efficiency on flowers. Female bees set 93% of fruit after a single visit. These findings guarantee their importance as pollinators and the persistence of the specialized plant-pollinator association.

Molecular mechanisms of mutualistic and antagonistic interactions in a plant-pollinator association.

Many insects metamorphose from antagonistic larvae into mutualistic adult pollinators, with reciprocal adaptation leading to specialized insect-plant associations. It remains unknown how such interactions are established at molecular level. Here we assemble high-quality genomes of a fig species, Ficus pumila var. pumila, and its specific pollinating wasp, Wiebesia pumilae. We combine multi-omics with validation experiments to reveal molecular mechanisms underlying this specialized interaction. In the plant, we identify the specific compound attracting pollinators and validate the function of several key genes regulating its biosynthesis. In the pollinator, we find a highly reduced number of odorant-binding protein genes and an odorant-binding protein mainly binding the attractant. During antagonistic interaction, we find similar chemical profiles and turnovers throughout the development of galled ovules and seeds, and a significant contraction of detoxification-related gene families in the pollinator. Our study identifies some key genes bridging coevolved mutualists, establishing expectations for more diffuse insect-pollinator systems.

Potential regional declines in species richness of tomato pollinators in North America under climate change.

About 70% of the world's main crops depend on insect pollination. Climate change is already affecting the abundance and distribution of insects, which could cause geographical mismatches between crops and their pollinators. Crops that rely primarily on wild pollinators (e.g., crops that cannot be effectively pollinated by commercial colonies of honey bees) could be particularly in jeopardy. However, limited information on plant-pollinator associations and pollinator distributions complicate the assessment of climate change impacts on specific crops. To study the potential impacts of climate change on pollination of a specific crop in North America, we use the case of open-field tomato crops, which rely on buzz pollinators (species that use vibration to release pollen, such as bumble bees) to increase their production. We aimed to (1) assess potential changes in buzz pollinator distribution and richness, and (2) evaluate the overlap between areas with high densities of tomato crops and high potential decrease in richness. We used baseline (1961-1990) climate and future (2050s and 2080s) climatic projections in ecological niche models fitted with occurrences of wild bees, documented in the literature as pollinators of tomatoes, to estimate the baseline and future potential distribution of suitable climatic conditions of targeted species and to create maps of richness change across North America. We obtained reliable models for 15 species and found important potential decreases in the distribution of some pollinators (e.g., Lasioglossum pectorale and Augochlorella aurata). We observed geographical discrepancies in the projected change in species richness across North America, detecting important declines in the eastern United States (up to 11 species decrease for 2050s). After overlapping the maps of species richness change with a tomato crop map for the United States, we found spatial correspondence between richness declines and areas with high concentration of tomato crops. Disparities in the effects of climate change on the potential future distribution of different wild pollinators and geographical variation in richness highlight the importance of crop-specific studies. Our study also emphasizes the challenges of compiling and modeling crop-specific pollinator data and the need to improve our understanding of current distribution of pollinators and their community dynamics under climate change.

Effects of Urbanization on Plant-Pollinator Interactions in the Tropics: An Experimental Approach Using Exotic Plants.

Simple SummaryIsland environments of the Southwest Pacific, like New Caledonia, generally present poorly diversified bee fauna. Thus, they are particularly prone to the establishment of introduced bee species. These exotic species may compete with native bees for plant resources, disrupt pollination of native plants, and enhance the reproduction of exotic ones. To conserve local plant–pollinator interactions, it is essential to assess the factors favoring the presence and the activity of exotic bees. Here, we focused on the effects of urbanization on plant–pollinator interactions. We set up experimental plant communities composed of four exotic species in two contrasted habitats—a natural environment vs. an urban environment—and observed plant–pollinator interactions. We showed that the urban environment was largely dominated by exotic bees. We also showed that some exotic bee species can interact preferentially with a single exotic ornamental plant species. Overall, our results indicate that Nouméa is an entry point for exotic bees, which should encourage local authorities to maintain biosecurity measures to effectively limit the arrival of exogenous bees. Lastly, the use of exotic horticultural plants in green public spaces should be questioned regarding their potential attractiveness to exotic bees.Land-use changes through urbanization and biological invasions both threaten plant-pollinator networks. Urban areas host modified bee communities and are characterized by high proportions of exotic plants. Exotic species, either animals or plants, may compete with native species and disrupt plant–pollinator interactions. These threats are heightened in insular systems of the Southwest Pacific, where the bee fauna is generally poor and ecological networks are simplified. However, the impacts of these factors have seldom been studied in tropical contexts. To explore those questions, we installed experimental exotic plant communities in urban and natural contexts in New Caledonia, a plant diversity hotspot. For four weeks, we observed plant–pollinator interactions between local pollinators and our experimental exotic plant communities. We found a significantly higher foraging activity of exotic wild bees within the city, together with a strong plant–pollinator association between two exotic species. However, contrary to our expectations, the landscape context (urban vs. natural) had no effect on the activity of native bees. These results raise issues concerning how species introduced in plant–pollinator networks will impact the reproductive success of both native and exotic plants. Furthermore, the urban system could act as a springboard for alien species to disperse in natural systems and even invade them, leading to conservation concerns.

New directions in pollinator research: diversity, conflict and response to global change.

Interactions between pollinators and their plant hosts are central to maintaining global biodiversity and ensuring our food security. In this special issue, we compile reviews that summarize existing knowledge and point out key outstanding research areas to understand and safeguard pollinators, pollinators-host plant interactions and the pollination ecosystem services they provide. The vast diversity of the pollinator-plant interactions that exists on this planet still remains poorly explored, with many being associations involving a specialist pollinator partner, although historically most focus has been given to generalist pollinators, such as the honeybee. Two areas highlighted here are the ecology and evolution of oligolectic bee species, and the often-neglected groups of pollinators that forage solely at night. Advances in automated detection technologies could offer potential and complementary solutions to the current shortfall in knowledge on interactions occurring between less well-documented plant-pollinator associations, by increasing the collection range and capacity of flower visitation data over space and time. Pollinator-host plant interactions can be affected by external biotic factors, with herbivores and pathogens playing particularly important roles. Such interactions can be disrupted by modifying plant volatile and reward chemistry, with possible effects on pollinator attraction and pollination success. Mechanisms which underpin interactions between plants and their pollinators also face many anthropogenic disturbances. Reviews in this issue discuss threats from parasites and climate change to pollinator populations and plant-pollinator networks, and suggest new ways to mitigate these threats. While the protection of existing plant-pollinator networks will be a crucial goal for conservation biology, more research is needed to understand how lost interactions in degraded habitats may be restored with mutual benefits to plants and pollinators.

Seasonal variation of a plant-pollinator network in the Brazilian Cerrado: Implications for community structure and robustness.

Seasonal variation in the availability of floral hosts or pollinators is a key factor influencing diversity in plant-pollinator communities. In seasonally dry Neotropical habitats, where month-long periods of extreme drought are followed by a long rainy season, flowering is often synchronized with the beginning of precipitation, when environmental conditions are most beneficial for plant reproduction. In the Brazilian Cerrado, a seasonally dry ecosystem considered one of the world’s biodiversity hotspots for angiosperms, plants with shallow root systems flower predominantly during the rainy season. Foraging activity in social bees however, the major pollinators in this biome, is not restricted to any particular season because a constant supply of resources is necessary to sustain their perennial colonies. Despite the Cerrado’s importance as a center of plant diversity, the influence of its extreme cycles of drought and precipitation on the dynamics and stability of plant-pollinator communities is not well understood. We sampled plant-pollinator interactions of a Cerrado community weekly for one year and used network analyses to characterize intra-annual seasonal variation in community structure. We also compared seasonal differences in community robustness to species loss by simulating extinctions of plants and pollinators. We find that the community shrinks significantly in size during the dry season, becoming more vulnerable to disturbance due to the smaller pool of floral hosts available to pollinators during this period. Major changes in plant species composition but not in pollinators has led to high levels of turnover in plant-pollinator associations across seasons, indicated by in interaction dissimilarity (<3% of shared interactions). Aseasonal pollinators, which mainly include social bees and some solitary specialized bees, functioned as keystone species, maintaining robustness during periods of drastic changes in climatic conditions.

Effects of Plant Diversity, Vegetation Composition, and Habitat Type on Different Functional Trait Groups of Wild Bees in Rural Beijing.

The loss of flower-rich habitats and agricultural intensification have resulted in significant losses of wild bee diversity from agricultural landscapes that is increasingly threatening the pollination of zoochorous agricultural crops and agricultural sustainability. However, the links of different wild bee functional trait groups with habitat types and plant resources in agricultural landscapes remain poorly understood, thus impeding the formulation of effective policies for bee conservation. We therefore analyzed how bees representing different functional groups responded to variations in habitat type, vegetation composition and plant diversity. Natural shrubland sustained the highest diversity in bees overall, in large-sized bees, solitary bees and belowground-nesting bees, while each habitat harbored unique species. In half of the functional bee groups, species were negatively linked to tree coverage and herb coverage, respectively, while plant diversity was positively related to all functional groups except large-sized bees and aboveground-nesting bees. Overall bee abundance was positively related to abundance of plants in the Sympetalae, and negatively related to abundance of plants in the Archichlamydeae. Different bee functional groups showed distinct preferences for different plant communities. In order to conserve the diversity of wild bees across functional groups to optimize associated pollination services, a diverse habitat mosaic, and particularly plant species in Sympetalae need to be promoted in agricultural landscapes. Future studies should aim to enhance our understanding of plant-pollinator associations and specific food requirement of different wild bee species for their effective conservation.

Cophylogenetic signal is detectable in pollination interactions across ecological scales.

That evolutionary history can influence the way that species interact is a basic tenet of evolutionary ecology. However, when the role of evolution in determining ecological interactions is investigated, focus typically centers on just one side of the interaction. A cophylogenetic signal, the congruence of evolutionary history across both sides of an ecological interaction, extends these previous explorations and provides a more complete picture of how evolutionary patterns influence the way species interact. To date, cophylogenetic signal has most typically been studied in interactions that occur between fine taxonomic clades that show high intimacy. In this study, we took an alternative approach and made an exhaustive assessment of cophylogeny in pollination interactions. To do so, we assessed the strength of cophylogenetic signal at four distinct scales of pollination interaction: (1) across plant-pollinator associations globally, (2) in local pollination communities, (3) within the modular structure of those communities, and (4) in individual modules. We did so using a globally distributed dataset comprised of 54 pollination networks, over 4000 species, and over 12,000 interactions. Within these data, we detected cophylogenetic signal at all four scales. Cophylogenetic signal was found at the level of plant-pollinator interactions on a global scale and in the majority of pollination communities. At the scale defined by the modular structure within those communities, however, we observed a much weaker cophylogenetic signal. Cophylogenetic signal was detectable in a significant proportion of individual modules and most typically when within-module phylogenetic diversity was low. In sum, the detection of cophylogenetic signal in pollination interactions across scales provides a new dimension to the story of how past evolution shapes extant pollinator-angiosperm interactions.

Pollinator type and secondarily climate are related to nectar sugar composition across the angiosperms

Pollinators are important agents of selection on floral traits, including nectar sugar composition. Although it is widely assumed that the proportion of sugars (mainly sucrose, glucose and fructose) in nectar reflects pollinators’ physiological limitations and digestive efficiency, the relative impact of pollinators and abiotic factors on nectar sugar composition, as well as the generality of these associations across the angiosperms, remain unknown. We compiled data on nectar sugar composition for >1000 plant species, along with information on flower visitors, plant growth form and latitudinal climatic zone, to provide the first comprehensive assessment of correlates of variation in sugar nectar composition in the angiosperms. After assembling a phylogeny linking all species in the dataset, we estimated the amount of phylogenetic signal in the percentage of sucrose and, by applying phylogenetically-informed multiple regressions, we evaluated whether nectar composition was influenced either by the main pollinator group, plant growth form, or latitudinal climatic zone. The relative importance of each of these factors was then assessed through model selection based on Akaike information criteria and deviance partitioning analysis. Nectar was dominated by sucrose in 56.8% of all the species, glucose in 16.7%, and fructose in 5.5%. Nectar in the remaining species was characterized by similar proportions of the three sugars. Variation in the proportion of sucrose was highest (~70%) at the intrafamily level, and had a significant but low phylogenetic signal, which partially reflects phylogenetic conservatism of the pollinator niche. After controlling for phylogenetic effects, the proportion of sucrose was mainly related to pollinator type and secondarily to climate. Accordingly, this study indicates that nectar sugar composition shows high evolutionary lability and its variation reflects plant-pollinator associations.

Pollinators show flower colour preferences but flowers with similar colours do not attract similar pollinators

Colour is one of the main floral traits used by pollinators to locate flowers. Although pollinators show innate colour preferences, the view that the colour of a flower may be considered an important predictor of its main pollinators is highly controversial because flower choice is highly context-dependent, and initial innate preferences may be overridden by subsequent associative learning. Our objective is to establish whether there is a relationship between flower colour and pollinator composition in natural communities. We measured the flower reflectance spectrum and pollinator composition in four plant communities (85 plant species represented by 109 populations, and 32305 plant-pollinator interactions in total). Pollinators were divided into six taxonomic groups: bees, ants, wasps, coleopterans, dipterans and lepidopterans. We found consistent associations between pollinator groups and certain colours. These associations matched innate preferences experimentally established for several pollinators and predictions of the pollination syndrome theory. However, flowers with similar colours did not attract similar pollinator assemblages. The explanation for this paradoxical result is that most flower species are pollination generalists. We conclude that although pollinator colour preferences seem to condition plant-pollinator interactions, the selective force behind these preferences has not been strong enough to mediate the appearance and maintenance of tight colour-based plant-pollinator associations.

Wild bee pollination networks in northern New England

Conserving and maintaining a diverse assemblage of wild bees is essential for a healthy and functioning ecosystem, as species are uniquely evolved to deliver specific plant–pollination requirements. Understanding the biology and ecology of bees in poorly studied regions is the first step towards conservation. Detailed surveys in New Hampshire reveal a broad diversity of 118 species of wild bees in different guilds and habitats including 17 bee species representing new state records. Network analyses reveal a complex community structure and relatively poorly connected plant–pollinator associations, thus species may be susceptible to disturbance. Phenological analyses document that at least one representative of five native bee families was present throughout the foraging season and both abundance and diversity were highest in June and July. This study provides important baseline information on bee abundance, diversity, phenology, and host plant associations necessary for future conservation efforts.

Dynamical transitions in a pollination-herbivory interaction: a conflict between mutualism and antagonism.

Plant-pollinator associations are often seen as purely mutualistic, while in reality they can be more complex. Indeed they may also display a diverse array of antagonistic interactions, such as competition and victim–exploiter interactions. In some cases mutualistic and antagonistic interactions are carried-out by the same species but at different life-stages. As a consequence, population structure affects the balance of inter-specific associations, a topic that is receiving increased attention. In this paper, we developed a model that captures the basic features of the interaction between a flowering plant and an insect with a larval stage that feeds on the plant’s vegetative tissues (e.g. leaves) and an adult pollinator stage. Our model is able to display a rich set of dynamics, the most remarkable of which involves victim–exploiter oscillations that allow plants to attain abundances above their carrying capacities and the periodic alternation between states dominated by mutualism or antagonism. Our study indicates that changes in the insect’s life cycle can modify the balance between mutualism and antagonism, causing important qualitative changes in the interaction dynamics. These changes in the life cycle could be caused by a variety of external drivers, such as temperature, plant nutrients, pesticides and changes in the diet of adult pollinators.

Multiple recent introductions of apid bees into Pacific archipelagos signify potentially large consequences for both agriculture and indigenous ecosystems

The islands of the south west Pacific (SWP) are highly biodiverse, yet records of their bee fauna suggest a region depauperate of a key pollinator suite. Studies of the bees of Fiji based on molecular data have revealed a recent origin with the majority of species having arrived since the last glacial maximum or introduced since human colonization. Here we use DNA barcodes to provide the first detailed account of Apidae bees from Vanuatu, Fiji, and Samoa. We show that most if not all species in these archipelagos have been recently introduced from Australia and south east Asia, with a further species introduced from the New World. Some of these species have become regionally abundant and we discuss the potential impact of introduced pollinators on endemic plant–pollinator associations. Given the wide-reaching role of native pollinators in island systems, yet lack of understanding of SWP pollinator suites, our study highlights the urgent need for more detailed pollinator research in the region.

Philodendron adamantinum(Araceae) lures its single cyclocephaline scarab pollinator with specific dominant floral scent volatiles

Cyclocephline scarabs and their host plants are documented as highly specialized plant–pollinator associations, with various fine-tuned adaptations. We studied the association between Philodendron adamantinum, a species endemic to the Espinhaço Range in Minas Gerais, South-East Brazil, and its exclusive pollinators. We focused on the pollination mechanism and reproductive success of P. adamantinum, analysed its floral scent composition, and performed field bioassays to verify the scent-mediated attraction of pollinators. The reproductive success of P. adamantinum depends on the presence of Erioscelis emarginata (Scarabaeidae, Cyclocephalini), its sole pollinator. At dusk, the inflorescences heat up to 18 °C above the surrounding ambient air temperature and give off a strong sweet odour, from which 32 volatile compounds were isolated. Dihydro-β-ionone, the major constituent in the floral scent bouquet, lures individuals of E. emarginata when applied to scented artificial decoys, either alone or blended with methyl jasmonate. We attribute the low fruit set of P. adamantinum at our study sites to pollinator limitation of small and isolated populations and geitonogamic pollen flow of vegetatively generated clonal plant groups. The interaction between P. adamantinum and E. emarginata shows common traits typical of the known plant–pollinator associations involving cyclocephaline scarabs: the asymmetrical dependence of plants on their pollinators, and the scent-mediated interaction between flowers and beetles. In addition to updating the current catalogue of active compounds of cantharophilous pollination systems, further experimental studies should elucidate the role of the specific chemical compounds that attract pollinators along different time and biogeographic scales.

Effects of gene flow on phenotype matching between two varieties of Joshua tree (Yucca brevifolia; Agavaceae) and their pollinators

In animal-pollinated plants, local adaptation to pollinator behaviour or morphology can restrict gene flow among plant populations; but gene flow may also prevent divergent adaptation. Here, we examine possible effects of gene flow on plant-pollinator trait matching in two varieties of Joshua tree (Agavaceae: Yucca brevifolia). The two varieties differ in strikingly in floral morphology, which matches differences in the morphology of their pollinators. However, this codivergence is not present at a smaller scale: within the two varieties of Joshua tree, variation in floral morphology between demes is not correlated with differences in moth morphology. We use population genetic data for Joshua tree and its pollinators to test the hypotheses that gene flow between Joshua tree populations is structured by pollinator specificity, and that gene flow within the divergent plant-pollinator associations 'swamps' fine-scale coadaptation. Our data show that Joshua tree populations are structured by pollinator association, but the two tree varieties are only weakly isolated - meaning that their phenotypic differences are maintained in the face of significant gene flow. Coalescent analysis of gene flow between the two Joshua tree types suggests that it may be shaped by asymmetric pollinator specificity, which has been observed in a narrow zone of sympatry. Finally, we find evidence suggesting that gene flow among Joshua tree sites may shape floral morphology within one plant-pollinator association, but not the other.

From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning.

Flower colour is a key component for plant signaling to pollinators and a staggering variety of colour variations are found in nature. Patterning of flower colour, such as pigment spots or stripes, is common and is important in promoting pollination success. Developmentally programmed pigmentation patterns are of interest with respect to the evolution of specialised plant-pollinator associations and as models for dissecting regulatory signaling in plants. This article reviews the occurrence and function of flower colour patterns, as well as the molecular genetics of anthocyanin pigmentation regulation. The transcription factors controlling anthocyanin biosynthesis have been characterised for many species and an 'MBW' regulatory complex of R2R3MYB, bHLH and WD-Repeat proteins is of central importance. In particular, R2R3MYBs are key determinants of pigmentation intensity and patterning in plants. Progress is now being made on how environmental or developmental signal pathways may in turn control the production of the MBW components. Furthermore, additional regulatory proteins that interact with the MBW activation complex are being identified, including a range of proteins that repress complex formation or action, either directly or indirectly. This review discusses some of the recent data on the regulatory factors and presents models of how patterns may be determined.

Pollen partitioning of three species of Convolvulaceae among oligolectic bees in the Caatinga of Brazil

During the rainy season many species of Convolvulaceae bloom simultaneously in the Caatinga of northeast Brazil. In a Caatinga nature reserve we studied pollination and breeding systems of three sympatric species of Convolvulaceae, Ipomoea bahiensis, I. nil, and Merremia aegyptia, focusing on pollen partitioning among flower visitors and pollen flow. The study showed that only oligolectic bees collected pollen and that these species had different preferences among the three species of Convolvulaceae: pollen of Ipomoea bahiensis, the only self-incompatible species, was collected mainly by Melitoma segmentaria, M. osmioides, and Melitomella murihirta; pollen of I. nil by Lithurgus huberi; and that of Merremia aegyptia by Ancyloscelis apiformis and an undescribed species of this genus. Introduced honey bees visited only flowers of Merremia aegyptia, where they were extraordinarily frequent flower visitors. However, they discarded the pollen grains, which led to almost 50% pollen loss. No polylectic bee species compete for pollen with the oligolectic species. Partitioning of pollen diminishes competition for floral resources in this specialized plant–pollinator association.

Ant aggression and evolutionary stability in plant-ant and plant-pollinator mutualistic interactions

Mutualistic partners derive a benefit from their interaction, but this benefit can come at a cost. This is the case for plant-ant and plant-pollinator mutualistic associations. In exchange for protection from herbivores provided by the resident ants, plants supply various kinds of resources or nests to the ants. Most ant-myrmecophyte mutualisms are horizontally transmitted, and therefore, partners share an interest in growth but not in reproduction. This lack of alignment in fitness interests between plants and ants drives a conflict between them: ants can attack pollinators that cross-fertilize the host plants. Using a mathematical model, we define a threshold in ant aggressiveness determining pollinator survival or elimination on the host plant. In our model we observed that, all else being equal, facultative interactions result in pollinator extinction for lower levels of ant aggressiveness than obligatory interactions. We propose that the capacity to discriminate pollinators from herbivores should not often evolve in ants, and when it does it will be when the plants exhibit limited dispersal in an environment that is not seed saturated so that each seed produced can effectively generate a new offspring or if ants acquire an extra benefit from pollination (e.g. if ants eat fruit). We suggest specific mutualism examples where these hypotheses can be tested empirically.

Cyto-nuclear discordance in the phylogeny of Ficus section Galoglychia and host shifts in plant-pollinator associations.

BackgroundHybridization events are relatively common in vascular plants. However, the frequency of these events is unevenly distributed across the plant phylogeny. Plant families in which individual species are pollinated by specific pollinator species are predicted to be less prone to hybridization than other families. However, exceptions may occur within these families, when pollinators shift host-plant species. Indeed, host shifts are expected to increase the rate of hybridization events. Pollinators of Ficus section Galoglychia are suspected to have changed host repeatedly, based on several cases of incongruence between plant phylogeny and taxonomy, and insect phylogeny and taxonomy. We tracked cyto-nuclear discordance across section Galoglychia as evidence for hybridization. To achieve a proper global view, we first clarified the monophyly of section Galoglychia as it had been questioned by recent phylogenetic studies. Moreover, we investigated if fig size could be a factor facilitating host shifts.ResultsPhylogenetic chloroplast and nuclear results demonstrated the monophyly of section Galoglychia. Within section Galoglychia, we detected several cases of statistically significant cyto-nuclear discordance. Discordances concern both terminal nodes of the phylogenetic trees and one deep node defining relationships between subsections. Because nuclear phylogeny is congruent with morphological taxonomy, discordances were caused by the chloroplast phylogeny. Introgressive hybridization was the most likely explanation for these discordances. We also detected that subsections pollinated by several wasp genera had smaller figs and were pollinated by smaller wasps than subsections pollinated by a single wasp genus.ConclusionAs hypothesized, we discovered evidences of past hybridization in Ficus section Galoglychia. Further, introgression was only detected in subsections presenting incongruence between plant and pollinator phylogenies and taxonomy. This supports the hypothesis that host shift is the cause for plant-pollinator incongruence. Moreover, small fig size could facilitate host shifts. Eventually, this study demonstrates that non-coding chloroplast markers are valuable to resolve deep nodes in Ficus phylogeny.