Floral Scent Evolution in the Genus Jaborosa (Solanaceae): Influence of Ecological and Environmental Factors.

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.

Flower Diversification Across "Pollinator Climates": Sensory Aspects of Corolla Color Evolution in the Florally Diverse South American Genus Jaborosa (Solanaceae).

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.

Phenotypic selection mosaic for flower length influenced by geographically varying hawkmoth pollinator proboscis length and abiotic environment.

Biotic and abiotic context may affect the intensity of interspecific interactions and subsequently drive locally particular phenotypic selection patterns on interacting traits. We evaluated the geographical variation of matching traits of the brush-type flowers of Caesalpinia gilliesii and of the proboscis length of its guild of hawkmoth pollinators, as well as their relationship with environmental variables. We assessed the geographical variation of interacting traits (style and filament vs mean proboscis length of the guild of hawkmoths) across seven populations and estimated phenotypic selection on the plant side. Interacting traits showed similar relationships with environmental variables. Phenotypic selection on the plant side was influenced by proboscis length and by environmental conditions. Mean proboscis length of the guild was shorter than previously recorded for the same study area, thus probably shifting the selective optima of flower length. We observed two presumptive coevolutionary cold spots where one-sided negative directional selection is acting on style length. The lack of selection on the pollinator side should be further confirmed. We provided joint evidence, mostly lacking, about the geographical variation of selective pressures on the plant side associated with both proboscis length and abiotic conditions. We suggest that recent environmental change may be shifting floral length optima.

Correction: Range overlap between the sword-billed hummingbird and its guild of long-flowered species: An approach to the study of a coevolutionary mosaic.

[This corrects the article DOI: 10.1371/journal.pone.0209742.].

Range overlap between the sword-billed hummingbird and its guild of long-flowered species: An approach to the study of a coevolutionary mosaic.

The coevolutionary process among free-living mutualists with extremely long matching traits may favor the formation of mutualistic interaction networks through coevolutionary escalation, complementarity and convergence. These networks may be geographically structured; the links among the species of a local network are shaped by the biotic composition of the community, thus creating selection mosaics at broader geographical scales. Therefore, to fully understand a coevolutionary process, it is crucial to visualize the geographical structure of the interaction network across the landscape. In this study we focused on the poorly known interaction system between Ensifera ensifera and its guild of long-flowered plant species. We combined occurrence data and environmental variables to predict E. ensifera distribution, in addition to range polygons available for plant species in order to evaluate the geographical variation in bill length and plant species richness. A positive relationship between bill length and plant species richness within the E. ensifera range suggests a geographical structuring of the interaction networks. At mid-latitude locations of E. ensifera range, where hummingbirds attained the longest bills, richness of long-flowered plant species was higher than at low latitude locations. These locations likely represent coevolutionary vortices where long-lasting reciprocal selection probably drove the evolution of long traits, consequently drawing new plant species into the coevolutionary network. Conversely, areas where the sword-billed hummingbird was absent or had shorter bills probably represent coevolutionary coldspots. Our results provide a first insight into this phenotypically specialized plant-pollinator network across the landscape and show candidate areas to test the predictions of the coevolutionary hypothesis, such as reciprocal selection.

The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks.

1. Proboscis length has been proposed as a key dimension of plant pollination niches, but this niche space has not previously been explored at regional and global scales for any pollination system. Hawkmoths are ideal organisms for exploring pollinator niches as they are important pollinators in most of the biodiverse regions of the earth and vary greatly in proboscis length, with some species having the longest proboscides of all insects. 2. Using datasets for nine biogeographical regions spanning the Old and New World, we ask whether it is possible to identify distinct hawkmoth pollination niches based on the frequency distribution of proboscis length, and whether these niches are reflected in the depths of flowers that are pollinated by hawkmoths. We also investigate the levels of specialization in hawkmoth pollination systems at the regional and community level using data from interaction network studies. 3. We found that most regional hawkmoth assemblages have bimodal or multimodal distributions of proboscis length, and that these are matched by similar distributions of floral tube lengths. Hawkmoths, particularly those with longer proboscides, are polyphagous and at the network level show foraging specialization equivalent to or less than that of bees and hummingbirds. In the case of plants, shorter-tubed flowers are usually visited by numerous hawkmoth species, while those that are longer-tubed tend to exclude shorter-proboscid hawkmoths and thus become ecologically specialized on longer-proboscid hawkmoth species. Longer-tubed flowers tend to have greater nectar rewards and this promotes short-term constancy by long-proboscid hawkmoths. 4. Our results show that pollinator proboscis length is a key niche axis for plants and can account for patterns of evolution in functional traits such as floral tube length and nectar volume. We also highlight a paradoxical trend for nectar resource niche breadth to increase according to proboscis length of pollinators, while pollinator niche breadth decreases according to the tube length of flowers.

Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks.

A major challenge in evolutionary ecology is to understand how co-evolutionary processes shape patterns of interactions between species at community level. Pollination of flowers with long corolla tubes by long-tongued hawkmoths has been invoked as a showcase model of co-evolution. Recently, optimal foraging models have predicted that there might be a close association between mouthparts' length and the corolla depth of the visited flowers, thus favouring trait convergence and specialization at community level. Here, we assessed whether hawkmoths more frequently pollinate plants with floral tube lengths similar to their proboscis lengths (morphological match hypothesis) against abundance-based processes (neutral hypothesis) and ecological trait mismatches constraints (forbidden links hypothesis), and how these processes structure hawkmoth-plant mutualistic networks from five communities in four biogeographical regions of South America. We found convergence in morphological traits across the five communities and that the distribution of morphological differences between hawkmoths and plants is consistent with expectations under the morphological match hypothesis in three of the five communities. In the two remaining communities, which are ecotones between two distinct biogeographical areas, interactions are better predicted by the neutral hypothesis. Our findings are consistent with the idea that diffuse co-evolution drives the evolution of extremely long proboscises and flower tubes, and highlight the importance of morphological traits, beyond the forbidden links hypothesis, in structuring interactions between mutualistic partners, revealing that the role of niche-based processes can be much more complex than previously known.

Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids.

BACKGROUND: Some species of long-spurred orchids achieve pollination by a close association with long-tongued hawkmoths. Among them, several Habenaria species present specialized mechanisms, where pollination success depends on the attachment of pollinaria onto the heads of hawkmoths with very long proboscises. However, in the Neotropical region such moths are less abundant than their shorter-tongued relatives and are also prone to population fluctuations. Both factors may give rise to differences in pollinator-mediated selection on floral traits through time and space. METHODOLOGY/PRINCIPAL FINDINGS: We characterized hawkmoth assemblages and estimated phenotypic selection gradients on orchid spur lengths in populations of three South American Habenaria species. We examined the match between hawkmoth proboscis and flower spur lengths to determine whether pollinators may act as selective agents on flower morphology. We found significant directional selection on spur length only in Habenaria gourlieana, where most pollinators had proboscises longer than the mean of orchid spur length. CONCLUSIONS/SIGNIFICANCE: Phenotypic selection is dependent on the mutual match between pollinator and flower morphologies. However, our findings indicate that pollinator-mediated selection may vary through time and space according to local variations in pollinator assemblages.

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

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