Nectar traits differ between pollination syndromes in Balsaminaceae.

BACKGROUND AND AIMS: The attractiveness of nectar rewards depends both on the quantity of nectar produced and on its chemical composition. It is known that nectar quantity and chemical composition can differ in plant species depending on the main pollinator associated with the species. The main aims of this study were to test formally whether nectar traits are adapted to pollination syndromes in the speciose Balsaminaceae and, if so, whether a combination of nectar traits mirrors pollination syndromes. METHODS: Comparative methods based on Ornstein-Uhlenbeck models were used to test whether nectar volume, nectar sucrose proportion, sugar and amino acid concentration and amino acid composition had evolved as a function of pollination syndromes in 57 species of Balsaminaceae. Cluster analysis and ordination were performed to derive clusters of species resembling each other in nectar composition. KEY RESULTS: Evolutionary models for nectar volume and nectar sucrose proportion performed best when including information on pollination syndrome, while including such information improve model fit neither for sugar and amino acid concentration nor for amino acid composition. A significant relationship emerged between pollination syndrome and the combined nectar traits. CONCLUSIONS: Our results show that nectar volume and nectar sucrose proportion evolve rapidly towards optimal values associated with different pollination syndromes. The detection of a signal indicating that nectar traits in combination are to a certain extent able to predict pollination syndromes in Balsaminaceae suggests that a holistic approach including the whole set of nectar traits helps us to better understand evolution of nectar composition in response to pollinators.

Breeding systems in Balsaminaceae in relation to pollen/ovule ratio, pollination syndromes, life history and climate zone.

Pollen/ovule (P/O) ratios are often used as proxy for breeding systems. Here, we investigate the relations between breeding systems and P/O ratios, pollination syndromes, life history and climate zone in Balsaminaceae. We conducted controlled breeding system experiments (autonomous and active self-pollination and outcrossing tests) for 65 Balsaminaceae species, analysed pollen grain and ovule numbers and evaluated the results in combination with data on pollination syndrome, life history and climate zone on a phylogenetic basis. Based on fruit set, we assigned three breeding systems: autogamy, self-compatibility and self-incompatibility. Self-pollination led to lower fruit set than outcrossing. We neither found significant P/O differences between breeding systems nor between pollination syndromes. However, the numbers of pollen grains and ovules per flower were significantly lower in autogamous species, but pollen grain and ovule numbers did not differ between most pollination syndromes. Finally, we found no relation between breeding system and climate zone, but a relation between climate zone and life history. In Balsaminaceae reproductive traits can change under resource or pollinator limitation, leading to the evolution of autogamy, but are evolutionary rather constant and not under strong selection pressure by pollinator guild and geographic range changes. Colonisation of temperate regions, however, is correlated with transitions towards annual life history. Pollen/ovule-ratios, commonly accepted as good indicators of breeding system, have a low predictive value in Balsaminaceae. In the absence of experimental data on breeding system, additional floral traits (overall pollen grain and ovule number, traits of floral morphology) may be used as proxies.

Pollinator adaptation and the evolution of floral nectar sugar composition.

A long-standing debate concerns whether nectar sugar composition evolves as an adaptation to pollinator dietary requirements or whether it is 'phylogenetically constrained'. Here, we use a modelling approach to evaluate the hypothesis that nectar sucrose proportion (NSP) is an adaptation to pollinators. We analyse ~ 2100 species of asterids, spanning several plant families and pollinator groups (PGs), and show that the hypothesis of adaptation cannot be rejected: NSP evolves towards two optimal values, high NSP for specialist-pollinated and low NSP for generalist-pollinated plants. However, the inferred adaptive process is weak, suggesting that adaptation to PG only provides a partial explanation for how nectar evolves. Additional factors are therefore needed to fully explain nectar evolution, and we suggest that future studies might incorporate floral shape and size and the abiotic environment into the analytical framework. Further, we show that NSP and PG evolution are correlated - in a manner dictated by pollinator behaviour. This contrasts with the view that a plant necessarily has to adapt its nectar composition to ensure pollination but rather suggests that pollinators adapt their foraging behaviour or dietary requirements to the nectar sugar composition presented by the plants. Finally, we document unexpectedly sucrose-poor nectar in some specialized nectarivorous bird-pollinated plants from the Old World, which might represent an overlooked form of pollinator deception. Thus, our broad study provides several new insights into how nectar evolves and we conclude by discussing why maintaining the conceptual dichotomy between adaptation and constraint might be unhelpful for advancing this field.

Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird.

A striking example of plant/pollinator trait matching is found between Andean species of Passiflora with 6-14-cm-long nectar tubes and the sword-billed hummingbird, Ensifera ensifera, with up to 11-cm-long bills. Because of the position of their anthers and stigmas, and self-incompatibility, these passionflower species depend on E. ensifera for pollination. Field observations show that the bird and plant distribution match completely and that scarcity of Ensifera results in reduced passionflower seed set. We here use nuclear and plastid DNA sequences to investigate how often and when these mutualisms evolved and under which conditions, if ever, they were lost. The phylogeny includes 26 (70%) of the 37 extremely long-tubed species, 13 (68%) of the 19 species with tubes too short for Ensifera and four of the seven bat-pollinated species for a total of 43 (69%) of all species in Passiflora supersection Tacsonia (plus 11 outgroups). We time-calibrated the phylogeny to infer the speed of any pollinator switching. Results show that Tacsonia is monophyletic and that its stem group dates to 10.7 Ma, matching the divergence at 11.6 Ma of E. ensifera from its short-billed sister species. Whether pollination by short-billed hummingbirds or by Ensifera is the ancestral condition cannot be securely inferred, but extremely long-tubed flowers exclusively pollinated by Ensifera evolved early during the radiation of the Tacsonia clade. There is also evidence of several losses of Ensifera dependence, involving shifts to bat pollination and shorter billed birds. Besides being extremely asymmetric-a single bird species coevolving with a speciose plant clade-the Ensifera/Passiflora system is a prime example of a specialized pollinator not driving plant speciation, but instead being the precondition for the maintenance of isolated populations (through reliable seed set) that then underwent allopatric speciation.