Covariance and decoupling of floral and vegetative traits in nine Neotropical plants: a re-evaluation of Berg's correlation-pleiades concept

Nearly forty years ago R. L. Berg proposed that plants with specialized pollination ecology evolve genetic and developmental systems that decouple floral morphology from phenotypic variation in vegetative traits. These species evolve separate floral and vegetative trait clusters, or as she termed them, "correlation pleiades." The predictions of this hypothesis have been generally supported, but only a small sample of temperate-zone herb and grass species has been tested. To further evaluate this hypothesis, especially its applicability to plants of other growth forms, we examined the patterns of phenotypic variation and covariation of floral and vegetative traits in nine species of Neotropical plants. We recognized seven specific predictions of Berg's hypothesis. Our results supported some predictions but not others. Species with specialized pollination systems usually had floral traits decoupled (weak correlation; Canna and Eichornia) or buffered (relationship with shallow proportional slope; Calathea and Canna) from variation in vegetative traits. However, the same trend was also observed in three species with unspecialized pollination systems (Echinodorus, Muntingia, and Wedelia). One species with unspecialized pollination (Croton) and one wind-pollinated species (Cyperus) showed no decoupling or buffering, as predicted. While species with specialized pollination usually showed lower coefficients of variation for floral traits than vegetative traits (as predicted), the same was also true of species with unspecialized or wind pollination (unlike our prediction). Species with specialized pollination showed less variation in floral traits than did species with unspecialized or wind pollination, as predicted. However, the same was true of the corresponding vegetative traits, which was unexpected. Also in contrast to our prediction, plants with specialized pollination systems did not exhibit tighter phenotypic integration of floral characters than did species with generalized pollination systems. We conclude that the patterns of morphological integration among floral traits and between floral and vegetative traits tend to be species specific, not easily predicted from pollination ecology, and generally more complicated than R. L. Berg envisaged.     

Covariance of floral and vegetative traits in four species of Ranunculaceae: a comparison between specialized and generalized pollination systems

Theory predicts that tighter correlation between floral traits and weaker relationship between floral and vegetative traits more likely occur in specialized flowers than generalized flowers,favoring by precise fit with pollinators.However,traits and trait correlations frequently vary under different environments.Through detecting spatiotemporal variation in phenotypic traits (floral organ size and vegetative size) and trait correlations in four Ranunculaceae species,we examined four predictions.Overall,our results supported these predictions to a certain degree.The mean coefficient of variation (CV) of floral traits in two specialized species (Delphinium kamaonense and Aconitum gymnandrum) was marginally significantly lower than that of another two generalized species (Trollius ranunculoides and Anemone obtusiloba).The two specialized species also showed marginally significantly smaller CV in floral traits than vegetative size across the two species.The absolute mean correlation between floral and vegetative traits,or that between floral traits in species with specialized flowers was not significantly lower,or higher than that in generalized plants,weakly supporting the predictions.Furthermore,we documented a large variation in trait correlations of four species among different seasons and populations.Study of covariance of floral and vegetative traits will benefit from the contrast of results obtained from generalized and specialized pollination systems.     

Functional decoupling between flowers and leaves in the Ameroglossum pernambucense complex can facilitate local adaptation across a pollinator and climatic heterogeneous landscape

Decoupling between floral and leaf traits is expected in plants with specialized pollination systems to assure a precise flower–pollinator fit, irrespective of leaf variation associated with environmental heterogeneity (functional modularity). Nonetheless, developmental interactions among floral traits also decouple flowers from leaves regardless of selection pressures (developmental modularity). We tested functional modularity in the hummingbird‐pollinated flowers of the Ameroglossum pernambucense complex while controlling for developmental modularity. Using two functional traits responsible for flower–pollinator fit [floral tube length (TL) and anther–nectary distance (AN)], one floral trait not linked to pollination [sepal length (SL), control for developmental modularity] and one leaf trait [leaf length (LL)], we found evidence of flower functional modularity. Covariation between TL and AN was ca. two‐fold higher than the covariation of either of these traits with sepal and leaf lengths, and variations in TL and AN, important for a precise flower–pollinator fit, were smaller than SL and LL variations. Furthermore, we show that previously reported among‐population variation of flowers associated with local pollinator phenotypes was independent from SL and LL variations. These results suggest that TL and AN are functionally linked to fit pollinators and sufficiently decoupled from developmentally related floral traits (SL) and vegetative traits (LL). These results support previous evidences of population differentiation due to local adaptation in the A. pernambucense complex and shed light on the role of flower–leaf decoupling for local adaptation in species distributed across biotic and abiotic heterogeneous landscapes.     

The movement of involucral bracts of Syngonanthus elegans (Eriocaulaceae-Poales): Anatomical and ecological aspects

Syngonanthus elegans flowers are distributed in capitula whose involucral bracts open and close in a diurnal rhythm. The anatomy of these bracts was studied to understand how such movements occur and how it influences reproductive ecology of the species. The involucral bracts have a single layered epidermis composed of thick-walled cells on the abaxial surface, which are responsible for the movement. Since they are hygroscopic, these cells swell when they absorb water from the surrounding environment, causing the bracts to bend and the capitula to close. In natural conditions, the capitula open by day, when temperature increases and the relative air humidity decreases, and close at night, when temperature decreases and the relative air humidity increases. The involucral bracts may thus protect the flowers from abiotic factors, exposing them only at the time of the day when temperature is higher and insects are more active, favoring pollination by small insects. The closed capitula do not only protect the flowers, but they also function as a shelter for floral visitors as Brachiacantha australe (Coccinellidae) and Eumolpini sp. (Chrysomelidae). These small Coleoptera pollinate the flowers of S. elegans during the day and remain within the closed capitula during the night, in a possible mutualistic relationship.     

Comparative floral biology of Rhynchospora ciliata (Vahl) Kukenth and R. pubera (Vahl) Boeckeler (Cyperaceae): the role of white involucral bracts in attracting pollinating insects

Although Cyperaceae are considered anemophilous, some species exhibit features that are attractive to pollinators, such as the white UV‐reflecting involucral bracts of Rhynchospora ciliata. But how effective are these conspicuous adaptations? To address this question, we tested the hypothesis that species such as R. ciliata are visited by greater numbers of pollinating insects than similar species with green involucral bracts, such as R. pubera. We compared the floral biology of both species and the number of visits to sympatric populations of each species, associating them with the availability of pollen and the pollination system. We verified that species with white involucral bracts are preferred, because there were more visits to R. ciliata in the first 2 h the flowers were open. The peak visitation in R. pubera was 2 h after the flowers opened, when the pollen of R. ciliata was exhausted. Although the involucral bracts of R. pubera are green, the spikelet scales and anthers are white and reflect ultraviolet light. Overall, flowers of R. pubera exhibit fewer white or reflective surfaces and are probably less conspicuous to a bee than those of R. ciliata. It is possible that R. pubera is a second option for visitors after the first 2 h of anthesis. The two different peaks in visitation minimize interspecific competition for pollinators, suggesting that R. ciliata and R. pubera together could attract more generalist pollinators and, instead of competing, facilitate the pollination of both species. Although R. pubera is autogamous and self‐compatible, both wind and insects are important to its reproductive success.     

Resource heterogeneity, diet shifts and intra-cohort competition: effects on size divergence in YOY fish

The pollination syndrome hypothesis has provided a major conceptual framework for how plants and pollinators interact. However, the assumption of specialization in pollination systems and the reliability of floral traits in predicting the main pollinators have been questioned recently. In addition, the relationship between ecological and evolutionary specialization in pollination interactions is still poorly understood. We used data of 62 plant species from three communities across southern Norway to test: (1) the relationships between floral traits and the identity of pollinators, (2) the association between floral traits (evolutionary specialization) and ecological generalization, and (3) the consistency of both relationships across communities. Floral traits significantly affected the identity of pollinators in the three communities in a way consistent with the predictions derived from the pollination syndrome concept. However, hover flies and butterflies visited flowers with different shapes in different communities, which we mainly attribute to among-community variation in pollinator assemblages. Interestingly, ecological generalization depended more on the community-context (i.e. the plant and pollinator assemblages in the communities) than on specific floral traits. While open yellow and white flowers were the most generalist in two communities, they were the most specialist in the alpine community. Our results warn against the use of single measures of ecological generalization to question the pollination syndrome concept, and highlight the importance of community comparisons to assess the pollination syndromes, and to understand the relationships between ecological and evolutionary specialization in plant-pollinator interactions.     

IS FLORAL SPECIALIZATION AN EVOLUTIONARY DEAD‐END? POLLINATION SYSTEM TRANSITIONS IN RUELLIA (ACANTHACEAE)

Pollination systems frequently reflect adaptations to particular groups of pollinators. Such systems are indicative of evolutionary specialization and have been important in angiosperm diversification. We studied the evolution of pollination systems in the large genus Ruellia. Phylogenetic analyses, morphological ordinations, ancestral state reconstructions, and a character mapping simulation were conducted to reveal key patterns in the direction and lability of floral characters associated with pollination. We found significant floral morphological differences among species that were generally associated with different groups of floral visitors. Floral evolution has been highly labile and also directional. Some specialized systems such as hawkmoth or bat pollination are likely evolutionary dead-ends. In contrast, specialized pollination by hummingbirds is clearly not a dead-end. We found evidence for multiple reverse transitions from presumed ancestral hummingbird pollination to more derived bee or insect pollination. These repeated origins of insect pollination from hummingbird-pollinated ancestors have not evolved without historical baggage. Flowers of insect-pollinated species derived from hummingbird-pollinated ancestors are morphologically more similar to hummingbird flowers than they are to other more distantly related insect-pollinated flowers. Finally, some pollinator switches were concomitant with changes in floral morphology that are associated with those pollinators. These observations are consistent with the hypothesis that some transitions have been adaptive in the evolution of Ruellia.     

Pollinator‐mediated selection in a specialized pollination system: matches and mismatches across populations

Most studies on pollinator‐mediated selection have been performed in generalized rather than specialized pollination systems. This situation has impeded evaluation of the extent to which selection acts on attraction or specialized key floral traits involved in the plant‐pollinator phenotypic interphase. We studied pollinator‐mediated selection in four populations of Nierembergia linariifolia, a self‐incompatible and oil‐secreting plant pollinated exclusively by oil‐collecting bees. We evaluated whether floral traits experience variable selection among populations and whether attraction and fit traits are heterogeneously selected across populations. Populations differed in every flower trait and selection was consistently observed for corolla size and flower shape, two traits involved in the first steps of the pollination process. However, we found no selection acting on mechanical‐fit traits. The observation that selection occurred upon attraction rather than mechanical‐fit traits, suggests that plants are not currently evolving fine‐tuned morphological adaptations to local pollinators and that phenotypic matching is not necessarily an expected outcome in this specialized pollination system.     

Staminode of Jacaranda rugosa A.H. Gentry (Bignoniaceae) promotes functional specialization by ensuring signaling and mechanical fit to medium-sized bees

Organisms Diversity & Evolution - The floral traits in Bignoniaceae are claimed as precise determiners of specialized pollination systems. Here, we investigated how such floral traits ensure a...     

REPRODUCTIVE BIOLOGY OF APIACEAE. II. CRYPTIC SPECIALIZATION AND FLORAL EVOLUTION IN THASPIUM AND ZIZIA

The classification of specialized floral syndromes has imposed a bias in the interpretation of pollination systems which may be either more generalized, or more specialized, than we have universally acknowledged. An analysis of floral biology in two umbellifer genera, Thaspium and Zizia, was undertaken in order to determine the extent to which cryptic floral or inflorescence variations determine pollination specialization despite a broad visitor spectrum and open reward system. Separate analyses were made of the primary attractants, nectar and pollen, and the secondary attractants, floral color and floral and inflorescence structure in conjunction with analyses of pollinator movements, stigmatic pollen loads and fruit set. All data support the conclusion that cryptic variation in floral and inflorescence characters enhance specialization for pollination by solitary bees or syrphid flies. In addition, evidence is presented for the importance of the oligolectic relationship between taxa of Thaspium and Zizia and the solitary bee, Andrena ziziae. The need for more experimental work both to further define the oligolectic relationship and to understand how floral and inflorescence color and structure affect insect movements is especially revealed by this study. The degree of pollination specialization in Thaspium and Zizia is not uncommon in Apiaceae and has important implications for floral evolution in this family and other plant groups with pollination systems categorized as “promiscuous.”     

Testing hypotheses of functional relationships: a comparative survey of correlation patterns among floral traits in five insect-pollinated plants

To test hypotheses on the evolution of functional relationships, phenotypic correlations among floral traits were estimated in five species of insect-pollinated plants. The species studied were wild radish (Raphanus raphanistrum), canola (Brassica napus), phlox (Phlox divaricata), dame's rocket (Hesperis matronalis), and black mustard (Brassica nigra). Six floral traits were measured on each species. In three of the five species the correlations between the filaments and corolla tube were significantly greater than the other floral correlations. This result is consistent with the hypothesis that selection for proper anther placement to enhance pollination has increased the filament-corolla tube correlations in these three species. In contrast, none of the species showed evidence of selection for an optimal stigma placement; the correlations between the pistil and corolla tube lengths were not greater than the other floral correlations in any of the five species.     

Back to the past for pollination biology

Manipulations of the interactions between plants and their floral visitors remain the most successful path to an understanding of floral traits, which may have been shaped by both herbivores and pollinators. By using genetic tools in combination with old-fashioned field work the dual protective/advertisement functions of floral traits are being realized. The distinction between wanted and unwanted floral visitors is blurring, and plants with specialized pollination systems are being found capable of using alternative pollinators if the specialized pollinators fail to perform.     

Genetic constraints on floral evolution: a review and evaluation of patterns

The characteristics of flowers influence most aspects of angiosperm reproduction, including the agents of pollination and patterns of mating. Thus, a clear view of the forces that mediate floral phenotypic evolution is central to understanding angiosperm diversity. Here, we inform on the capacity for floral phenotype to respond to selection by reviewing published data on heritabilities and genetic correlations for several classes of floral traits (primary sexual, attraction, mating system) in hermaphroditic plants. We find significant heritability for all floral traits but also variation among them, as well as a tendency for heritability to vary with mating system, but not life history. We additionally test predictions stemming from life history theory (eg, negative covariation between male-female traits and flower size-flower number), and ideas concerning the extent and pattern of genetic integration between flowers and leaves, and between the sexes of dioecious and gynodioecious species. We find mixed evidence for life history tradeoffs. We find strong support for floral integration and its relation with floral morphology (actinomorphy vs zygomorphy) and for a decoupling of floral and vegetative traits, but no evidence that modular integration varies with floral morphology. Lastly, we find mixed evidence for a relationship between the level of sexual dimorphism in attraction traits and the between-sex correlation in gender dimorphic plants.     

Floral and vegetative morphometrics of five Pleurothallis (Orchidaceae) species: correlation with taxonomy,phylogeny, genetic variability and pollination systems

Morphometric analyses of vegetative and floral characters were conducted in 21 populations of five Pleurothallis (Orchidaceae) species occurring in Brazilian 'campo rupestre' vegetation. A phylogenetic analysis of this species group was also carried out using nuclear ribosomal DNA internal transcribed spacers (ITS1 and ITS2). Results of the ordination and cluster analyses agree with species' delimitation revealed by taxonomic and allozyme studies. The groups formed in ordination analysis correspond to the pollinator groups determined in a previous pollination study. Relationships among the species in the cluster analysis using only vegetative characters are similar to those found in a previous allozyme study, but those indicated by cluster analysis using only floral characters differ. These results support the hypothesis that floral similarities are due to convergence driven by similar pollination mechanisms, and therefore floral traits may not be good indicators of phylogenetic relationships in this group. The results of the phylogenetic analysis support this conclusion to some extent. There is no correlation between genetic (allozyme) and morphological variability in the populations nor in the way this variability is distributed among conspecific populations. We describe a new subspecies of Pleurothallis ochreata based on differences in vegetative and chemical characters as well as geographic distribution. Absence of differentiation in floral characters, attraction of the same pollinator species, interfertility and genetic similarity support the argument for subspecific rather than specific status.     

Raissa L. Berg's contributions to the study of phenotypic integration,with a professional biographical sketch

Raissa L. Berg had a remarkable career in many respects and an impact on the study of phenotypic integration that continues to increase over 50 years after the publication of her seminal paper in that area. She was born and lived most of her life in Russia, with most of her research focused on measuring spontaneous mutation rates in Drosophila. She was forced to abandon this work during the height of Lysenko''s power in Russia, so she turned temporarily to the study of correlation patterns in plants; ironically, this work has had a more enduring impact than her main body of research. She showed that floral and vegetative traits become decoupled into separate correlation ‘pleiades’ in plants with specialized pollinators, but floral and vegetative traits remain correlated in plants that have less specialized pollination. Unfortunately, her plant work is often mis-cited as providing evidence for increased correlations among floral traits due to selection by pollinators for functional integration, a point she never made and one that is not supported by her data. Still, many studies of correlation pleiades have been conducted in plants, with the results mostly supporting Berg''s hypothesis, although more studies on species with generalized pollination are needed.     

Pollinators and seed predators generate conflicting selection on Dalechampia blossoms

Plant–pollinator relationships are often mediated by floral traits that advertise the presence or amount of rewards. However, herbivores may also use these traits to find their hosts. In Dalechampia scandens, we tested whether floral advertisements that attract pollinators were also used by seed predators, and whether this generated conflicting selection pressures. We studied the influence of natural variation in the size of showy bracts, amount of reward, and two shape traits on pollinator visitation, pollen arrival on stigmas, seed production and seed predation. We then built a multivariate fitness function for these traits to estimate selection generated by pollinators and seed predators. Blossoms with larger bracts were visited by bees more frequently and received more pollen on their stigmas. Seed predators laid more eggs on blossoms with larger bracts and also on blossoms later producing more seeds. Consequently, selection for larger bract size exerted by pollinators was counteracted by the selection exerted by seed predators. As a result, net selection on bract size tended to be stabilizing. Additionally, we found selection on traits that increased the rate of self‐pollination (assuming uniform seed quality). These results illustrate the importance of both mutualists and antagonists in floral evolution, as well as the value of taking an integrative approach to assessing selection on floral traits.     

Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture

Summary Morphological variation within organisms is integrated and often modular in nature. That is to say, the size and shape of traits tend to vary in a coordinated and structured manner across sets of organs or parts of an organism. The genetic basis of this morphological integration is largely unknown. Here, we report on quantitative trait loci (QTL) analysis of leaf and floral organ size in Arabidopsis thaliana. We evaluate patterns of genetic correlations among traits and perform whole-genome scans using QTL mapping methods. We detected significant genetic variation for the size and shape of each floral and leaf trait in our study. Moreover, we found large positive genetic correlations among sets of either flower or leaf traits, but low and generally nonsignificant genetic correlations between flower and leaf traits. These results support the hypothesis of independent floral and vegetative modules. We consider co-localization of QTL for different traits as support for a pleiotropic basis of morphological integration and modularity. A total of eight QTL affecting flower and three QTL affecting leaf traits were identified. Most QTL affected either floral or leaf traits, providing a general explanation for high correlations within and low correlations between modules. Only two genomic locations affected both flower and leaf growth. These results are discussed in the context of the evolution of modules, pleiotropy, and the putative homologous relationship between leaves and flowers.     

Are deception-pollinated species more variable than those offering a reward?

In most pollination systems, animals transfer pollen among plants of a given species. Pollinator visitations do not come without cost, so plants usually offer a reward. However, the flowers of some plant species, mostly orchids, lack rewards and deceive animals into visiting their flowers. Deceptive species are thought to have high levels of variation in traits associated with advertisement and pollinator attraction, which have been attributed to genetic drift, or disruptive selection due to pollinator behavior. Rewarding species are assumed to have less variation due to stabilizing selection. We compared variability in floral morphology and fragrance composition between deceptive and rewarding species. Because both suites of traits are often linked with floral advertisement and pollinator attraction, we expected variation to be greater in species with deceptive pollination systems than in those offering rewards. We obtained floral morphology metrics for 20 deceptive species and 41 rewarding species native or naturalized in Puerto Rico, Venezuela, and Ecuador. Floral fragrances were sampled from eight deceptive species and four rewarding species. We found that the amplitude of variation in floral morphology and fragrance composition covaries significantly. Comparison of coefficients of variation for morphology indicated that, overall, deceptive species show significantly higher variation than rewarding species, and this pattern was also found among just orchids or just nonorchids. There were no statistical differences in morphological variation between orchids and nonorchids within a functional pollination group. Fragrance variation, measured by Jaccard distance, tended to be greater for deceptive species than for rewarding species. Although overlap in measures of variation occurs between the two groups, the data support the hypothesis that populations of deception-pollinated species are more variable than rewarding species in traits associated with pollinator attraction.     

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

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

Associations between floral specialization and species diversity: cause, effect, or correlation?

It has been proposed frequently, from Darwin’s time onwards, that specialized pollination increases speciation rates and thus the diversity of plant species (i.e. clade species richness). We suggest here that the correlation between clade species richness and floral specialization is real, but that clade species richness is frequently the cause, not the result of floral specialization. We urge a broader, variance-partitioning perspective for assessing the causes of this correlation by suggesting four models of how the diversity-specialization correlation might come about: (1) floral specialization promotes initial reproductive isolation (“Initial-RI” model), (2) floral specialization promotes reinforcement of reproductive isolation upon secondary contact (“Reinforcement” model), (3) floral specialization reduces the extinction rate by promoting tighter species packing (“Extinction” model), (4) floral specialization is the result of high clade species richness, which increases the number of related species in communities, and thus selects for floral character displacement (“Character-Displacement” model). These hypotheses are evaluated by comparing the relationships between species richness, speciation mechanisms, and pollination precision, accuracy, and specialization in the broader literature and, more specifically, in four study systems: Dalechampia (Euphorbiaceae), Collinsia (Plantaginaceae), Burmeistera (Campanulaceae), and Stylidium (Stylidiaceae). These systems provide stronger support for the character-displacement hypothesis, wherein local species diversity drives the evolution of specialized pollination. Although the two reproductive-isolation hypotheses may hold for plants like orchids, with extremely precise pollination systems, the reproductive character-displacement hypothesis seems likely to be more important for plant groups with less precise pollination systems.