MACROEVOLUTIONARY TESTS OF POLLINATION SYNDROMES: A REPLY TO FENSTER ET AL.

Studies of floral ecology and evolution are often centered on the idea that particular floral trait combinations, or syndromes, represent adaptations for particular pollinators. Despite the conceptual importance of pollination syndromes, few macroevolutionary studies have statistically examined the relationship between pollinators and floral traits. Using 15 species of Iochroma, Smith et al. applied phylogenetically structured correlation analyses to test the relationship between floral variation and pollination system, quantified in terms of the importance of major pollinator groups. This study revealed that pollinator shifts are tied to changes in nectar reward and floral display but are not significantly correlated with changes in corolla length or color, contrary to what might be predicted from classical pollination syndromes. Fenster et al. question these findings because our pollinator importance estimates included recently introduced honey bees. To address this concern, we recalculated importance values excluding honey bees and repeated the analyses. We found the same patterns as in our original study with significant correlations between pollinators and nectar reward and display. We conclude that phylogenetic approaches provide essential tools for testing macroevolutionary predictions of pollination syndromes and, by applying these approaches to other radiations, we can refine our understanding of the role of pollinators in floral diversification.     

A quantitative review of pollination syndromes: do floral traits predict effective pollinators?

The idea of pollination syndromes has been largely discussed but no formal quantitative evaluation has yet been conducted across angiosperms. We present the first systematic review of pollination syndromes that quantitatively tests whether the most effective pollinators for a species can be inferred from suites of floral traits for 417 plant species. Our results support the syndrome concept, indicating that convergent floral evolution is driven by adaptation to the most effective pollinator group. The predictability of pollination syndromes is greater in pollinator‐dependent species and in plants from tropical regions. Many plant species also have secondary pollinators that generally correspond to the ancestral pollinators documented in evolutionary studies. We discuss the utility and limitations of pollination syndromes and the role of secondary pollinators to understand floral ecology and evolution.     

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.”     

Dissection of floral pollination syndromes in Petunia

Animal-mediated pollination is essential in the reproductive biology of many flowering plants and tends to be associated with pollination syndromes, sets of floral traits that are adapted to particular groups of pollinators. The complexity and functional convergence of various traits within pollination syndromes are outstanding examples of biological adaptation, raising questions about their mechanisms and origins. In the genus Petunia, complex pollination syndromes are found for nocturnal hawkmoths (P. axillaris) and diurnal bees (P. integrifolia), with characteristic differences in petal color, corolla shape, reproductive organ morphology, nectar quantity, nectar quality, and fragrance. We dissected the Petunia syndromes into their most important phenotypic and genetic components. They appear to include several distinct differences, such as cell-growth and cell-division patterns in the basal third of the petals, elongation of the ventral stamens, nectar secretion and nectar sugar metabolism, and enzymatic differentiation in the phenylpropanoid pathway. In backcross-inbred lines of species-derived chromosome segments in a transposon tagging strain of P. hybrida, one to five quantitative trait loci were identified for each syndrome component. Two loci for stamen elongation and nectar volume were confirmed in introgression lines and showed large allelic differences. The combined data provide a framework for a detailed understanding of floral syndromes from their developmental and molecular basis to their impact on animal behavior. With its molecular genetic tools, this Petunia system provides a novel venue for a pattern of adaptive radiation that is among the most characteristic of flowering plants.     

ASYMMETRIC EFFECTS OF LOSS AND GAIN OF A FLORAL TRAIT ON POLLINATOR PREFERENCE

Shifts in pollination syndromes involve coordinated changes in multiple floral traits. This raises the question of how plants can cope with rapid changes in pollinator availability by the slow process of accumulation of mutations in multiple genes. Here we study the transition from bee to hawkmoth pollination in the genus Petunia. Interspecific crosses followed by single locus introgressions were used to recreate putative intermediate evolutionary stages in the evolution of moth pollination. The effect of the loss/gain of petal color was asymmetric: it had no influence on the established pollinator but enhanced visitation by the new pollinator. Therefore, shifts in pollination syndromes may proceed through intermediate stages of reduced specialization and consequently enhanced reproductive assurance. The loss of petal color in moth‐pollinated Petunia involves null mutations in a single regulatory gene, An2. Such simple genetic changes may be sufficiently rapid and frequent to ensure survival during pollinator failure.     

Evolution of pollination syndromes and corolla symmetry in Balsaminaceae reconstructed using phylogenetic comparative analyses

Background and AimsFloral diversity as a result of plant–pollinator interactions can evolve by two distinct processes: shifts between pollination systems or divergent use of the same pollinator. Although both are pollinator driven, the mode, relative importance and interdependence of these different processes are rarely studied simultaneously. Here we apply a phylogenetic approach using the Balsaminaceae (including the species-rich genus Impatiens) to simultaneously quantify shifts in pollination syndromes (as inferred from the shape and colour of the perianth), as well as divergent use of the same pollinator (inferred from corolla symmetry).MethodsFor 282 species we coded pollination syndromes based on associations between floral traits and known pollination systems, and assessed corolla symmetry. The evolution of these traits was reconstructed using parsimony- and model-based approaches, using phylogenetic trees derived from phylogenetic analyses of nuclear ribosomal and plastid DNA sequence data.Key ResultsA total of 71 % of studied species have a bee pollination syndrome, 22 % a bimodal syndrome (Lepidoptera and bees), 3 % a bird pollination syndrome and 5 % a syndrome of autogamy, while 19 % of species have an asymmetrical corolla. Although floral symmetry and pollination syndromes are both evolutionarily labile, the latter shifts more frequently. Shifts in floral symmetry occurred mainly in the direction towards asymmetry, but there was considerable uncertainty in the pattern of shift direction for pollination syndrome. Shifts towards asymmetrical flowers were associated with a bee pollination syndrome.ConclusionFloral evolution in Impatiens has occurred through both pollination syndrome shifts and divergent use of the same pollinator. Although the former appears more frequent, the latter is likely to be underestimated. Shifts in floral symmetry and pollination syndromes depend on each other but also partly on the region in which these shifts take place, suggesting that the occurrence of pollinator-driven evolution may be determined by the availability of pollinator species at large geographical scales.     

开花式样对传粉者行为及花粉散布的影响

理解植物花的特征可以从单花特征和群体特征两个层次入手。开花式样是植物的花在群体上的特征体现, 通过在开花数目、开花类型以及花的排列上的变化, 不同的开花式样对传粉者具有不同的吸引力, 影响昆虫在植株上的活动, 使花粉运动的方向发生相应变化, 从而影响着植物最终的交配结果。此外开花式样随环境改变也会发生一些变化。本文介绍了开花式样研究的进展, 对开花数目、开花类型以及花的排列等3个方面的已有研究进行了分别阐述, 并提出开花式样研究应更多地考虑影响传粉的各种因素。     

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.     

Hybridization between pollination syndromes as an ecological and evolutionary resource

In plants, pollination syndromes (the correlated presence of many features of relevance to pollination mode, for instance pollination by a particular animal clade) are a striking feature of plant biodiversity, providing great floral phenotypic diversity (Fenster et al. 2004 ). Adaptation to a particular animal pollinator provides an explanation for why recently diverged plants can have such extreme differentiation in floral form. One might expect such elaborate adaptations to provide a high degree of pollinator specificity and hence reproductive isolation, but there are many cases where substantial gene flow exists between extreme floral morphs (see Table 1), and the resulting hybrids may be highly fertile. This gene flow provides tremendous opportunities to study the genetics and biology of the pollination syndromes by providing intermediate forms and segregating genotypes. If it is true that pollination syndromes result from adaptation under strong selection, we will expect such flowers to be crucibles of natural selection. If strong selection for particular floral phenotypes can be shown, then this, when coupled with hybridization, will give us one of the most valuable of all experimental systems for evolutionary research: gene flow and selection in balance. In this issue of Molecular Ecology, the paper of Milano et al. ( 2016 ) delivers this. It shows that in populations of the Ipomopsis aggregata complex, gene flow between pollination morphs is high and selection to stabilize those morphs is also high: a probable case of gene flow–selection balance.     

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.     

Pollination syndromes predict brood-site deceptive pollination by female hoverflies in Paphiopedilum dianthum (Orchidaceae)

In order to explore the relationship between the pollinator and pollination syndromes, and to evaluate the possibility of predicting likely pollinators based on pollination syndromes, the pollination biology of Paphiopedilum dianthum was examined. This species shares a close phylogenetic relationship, similar habit, and a recognizable syndrome of floral features (including helmet-shaped labellum, big dorsal sepal, and black warts or hairs on petals) with other brood-site deceptive Paphiopedilum species. According to the pollination syndrome concept, P. dianthum would be pollinated by hoverflies and attract pollinators with brood-site deception. Results were consistent with this prediction. Paphiopedilum dianthum was mainly pollinated by female hoverflies (Episyrphus balteatus), and these flies were indeed lured by the false brood-site on the orchid flower. It is suggested that the pollination syndrome may be correlated with pollination selective pressure, but not simply with pollinator species, and that accurate prediction requires consideration of all factors influencing floral characters, including habit and evolutionary history.     

Orchid pollination biology

Orchids display many unsurpassed floral specializations, as both rewarders and frauds in their interaction with animal pollinators. Accumulating evidence indicates that their floral evolution is driven by pollinator traits and that expenditure for maximized sexual reproduction is parcelled out over their lifetimes in strategies for coping with pollinator and resource limitations. Recent advances in orchid pollination biology center mainly on floral evolutionary processes, pseudocopulation and other deceptive pollination systems, and flower and fruit production in relation to costs of sexual reproduction.     

Isolation barriers between petunia axillaris and Petunia integrifolia (Solanaceae)

The isolation barriers restricting gene flow between populations or species are of crucial interest for understanding how biological species arise and how they are maintained. Few studies have examined the entire range of possible isolation barriers from geographic isolation to next generation hybrid viability. Here, we present a detailed analysis of isolation barriers between two flowering plant species of the genus Petunia (Solanaceae). Petunia integrifolia and P. axillaris feature divergent pollination syndromes but can produce fertile hybrids when crossed in the laboratory. Both Petunia species are primarily isolated in space but appear not to hybridize in sympatry. Our experiments demonstrate that pollinator isolation is very high but not strong enough to explain the absence of hybrids in nature. However, pollinator isolation in conjunction with male gametic isolation (i.e., pollen-pistil interaction) can explain the lack of natural hybridization, while postzygotic isolation barriers are low or nonexistent. Our study supports the notion that reproductive isolation in flowering plants is mainly caused by pre- rather than postzygotic isolation mechanisms.     

Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of<Emphasis Type="Italic"> Burmeistera cyclostigmata</Emphasis> and<Emphasis Type="Italic"> B. tenuiflora</Emphasis> (Campanulaceae)

In this study I documented the degree of specialization in the pollination systems of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae) to explore the potential role of floral isolation in the diversification of the genus. I asked which floral characteristics are important in specializing on either bat or hummingbird pollination, and whether overlap between these floral syndromes can exist. I examined nocturnal and diurnal pollen deposition, pollinator visitation rates, and single visit effectiveness and related them to intra- and interspecific variation in Burmeistera floral characteristics at Monteverde, Costa Rica. Bats and hummingbirds visited both Burmeistera species, and bats pollinated both species. Owing to differences in floral morphology, however, hummingbirds effectively pollinated only B. tenuiflora. The generalized pollination system of B. tenuiflora demonstrates that there can be overlap in the boundary between ornithophily and chiropterophily, and that nectar production and timing of anthesis do not serve as barriers between these syndromes. The high intraspecific variation in floral color from green to red or purple did not correlate with either nocturnal or diurnal pollen deposition. Degree of flower accessibility did affect pollination; nocturnal pollen deposition significantly decreased as flowers become more obstructed. In Burmeistera, floral morphology and accessibility appear to be the most important floral characteristics for specialization at the boundary between ornithophily and chiropterophily.     

Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest

BACKGROUND AND AIMS: Pollination is a critical stage in plant reproduction and thus in the maintenance and evolution of species and communities. The Caatinga is the fourth largest ecosystem in Brazil, but despite its great extent and its importance few studies providing ecological information are available, with a notable lack of work focusing on pollination biology. Here, general data are presented regarding the frequency of pollination systems within Caatinga communities, with the aim of characterizing patterns related to floral attributes in order to make possible comparisons with data for plant communities in other tropical areas, and to test ideas about the utility of syndromes. This paper also intends to provide a reference point for further studies on pollination ecology in this threatened ecosystem. METHODS: The floral traits and the pollination systems of 147 species were analysed in three areas of Caatinga vegetation in northeastern Brazil, and compared with world-wide studies focusing on the same subject. For each species, floral attributes were recorded as form, size, colour, rewards and pollination units. The species were grouped into 12 guilds according to the main pollinator vector. Analyses of the frequencies of the floral traits and pollination systems were undertaken. KEY RESULTS: Nectar and pollen were the most common floral resources and insect pollination was the most frequent, occurring in 69.9 % of the studied species. Of the entomophilous species, 61.7 % were considered to be melittophilous (43.1 % of the total). Vertebrate pollination occurred in 28.1 % of the species (ornithophily in 15.0 % and chiropterophily in 13.1 %), and anemophily was recorded in only 2.0 %. CONCLUSIONS: The results indicated that the pollination systems in Caatinga, despite climatic restrictions, are diversified, with a low percentage of generalist flowers, and similar to other tropical dry and wet forest communities, including those with high rainfall levels.     

Ecology and evolution of plant�Cpollinator interactions

Background

Some of the most exciting advances in pollination biology have resulted from interdisciplinary research combining ecological and evolutionary perspectives. For example, these two approaches have been essential for understanding the functional ecology of floral traits, the dynamics of pollen transport, competition for pollinator services, and patterns of specialization and generalization in plant–pollinator interactions. However, as research in these and other areas has progressed, many pollination biologists have become more specialized in their research interests, focusing their attention on either evolutionary or ecological questions. We believe that the continuing vigour of a synthetic and interdisciplinary field like pollination biology depends on renewed connections between ecological and evolutionary approaches.

Scope

In this Viewpoint paper we highlight the application of ecological and evolutionary approaches to two themes in pollination biology: (1) links between pollinator behaviour and plant mating systems, and (2) generalization and specialization in pollination systems. We also describe how mathematical models and synthetic analyses have broadened our understanding of pollination biology, especially in human-modified landscapes. We conclude with several suggestions that we hope will stimulate future research. This Viewpoint also serves as the introduction to this Special Issue on the Ecology and Evolution of Plant–Pollinator Interactions. These papers provide inspiring examples of the synergy between evolutionary and ecological approaches, and offer glimpses of great accomplishments yet to come.Key words: Floral traits, generalization and specialization, global change, male fitness, mating systems, multiple paternity, plant–pollinator networks, pollen and gene dispersal, pollinator behaviour, pollination syndromes, pollination webs, self-fertilization     

Relationships between species’ floral traits and pollinator visitation in a temperate grassland

Knowledge about plant–plant interactions for pollinator service at the plant community level is still scarce, although such interactions may be important to seed production and hence the population dynamics of individual plant species and the species compositions of communities. An important step towards a better understanding of pollination interactions at the community level is to assess if the variation in floral traits among plant species explain the variation in flower visitation frequency among those species. We investigated the relative importance of various floral traits for the visitation frequency of all insects, and bumblebees and flies separately, to plant species by measuring the visitation frequency to all insect-pollinated species in a community during an entire flowering season. Visitation frequency was identified to be strongly positive related to the visual display area and the date of peak flowering of plant species. Categorical variables, such as flower form and symmetry, were important to the visitation frequency of flies only. We constructed floral similarity measures based on the species’ floral traits and found that the floral similarity for all species’ traits combined and the continuous traits separately were positively related to individual visitation frequency. On the other hand, plant species with similar categorical floral traits did not have similar visitation frequencies. In conclusion, our results show that continuous traits, such as flower size and/or density, are more important for the variation in visitation frequency among plant species than thought earlier. Furthermore, differences in visitation frequency among pollinator groups give a poor support to the expectations derived from the classical pollination syndromes.     

Emission mechanism of floral scent in Petunia axillaris

The mechanism of floral scent emission was studied in Petunia axillaris, a plant with a diurnal rhythm of scent output. The emission rate of each volatile compound oscillated in synchrony with its endogenous concentration, so that the intensity of the floral scent appeared to be determined by the endogenous concentrations. The composition of major volatiles in the flower tissue and the flower headspace showed characteristic differences. A negative correlation was found between the boiling points of the volatile compounds and the ratio of their emitted and endogenous concentrations, indicating that the composition of the floral scent depends directly on the endogenous composition of the volatile compounds. We conclude that in P. axillaris, the physiological regulation of floral scent emission operates not in the vaporization process but in the control of the endogenous concentrations of volatiles through biosynthesis and metabolic conversion.