Evolutionary disruption in the pollination system of Vanilla (Orchidaceae)

Abstract

Pollination of the pantropical Vanilla has been linked to melittophily and food deception.• Here we investigated the role of flower traits on the reproduction of Neotropical Vanilla. We also studied the evolution of pollination systems in order to understand the origin of production of flower resources and the diversification of pollinators in this orchid genus. Our study was founded on data of adaptations in flower morphology, production of resources, scent release, pollinators and breeding systems of Vanilla and presenting new data on reproductive biology of V. palmarum. Data on reproductive biology of Vanilla were mapped onto a phylogeny to address our queries on the evolution of pollination systems in this genus.• Vanilla palmarum shows a mixed mating system, with its facultative autogamous flowers being pollinated by hummingbirds. Its yellow flowers are scentless and produces nectar. Mapping of the pollination system onto trees resulted in one origin for bird pollination and at least two origins for autogamy in Vanilla. Nectar secretion has a single origin in the Neotropical thick-leafed lineage.• Bird pollination of Vanilla is shown for the first time. The origin of ornithophily within a bee-pollinated clade is supported by flower morphology. Floral transitions to ornithophily have been favoured by the occupation of a distinct niche from that of the other thick-leafed Vanilla species. Despite its specialized pollination, V. palmarum is autogamous. A mixed mating system can promote reproductive assurance in the case of a decline in pollinator populations, or in areas where pollinator services are irregular or absent.

Vanilla beyond Vanilla planifolia and Vanilla × tahitensis: Taxonomy and Historical Notes, Reproductive Biology, and Metabolites

“…Species may exhibit different mating systems. To assess the breeding system of Vanilla species, different tests have been applied, such as (i) agamospermy, in which the pollen content was removed before the complete development of the flowers, as performed with V. bicolor flowers [ 33 ]; (ii) spontaneous self-pollination or autogamy experimentation, in which pre-anthesis buds are bagged for avoidance of a pollinator visit, using insect-proof bags; (iii) open pollination or control treatment, in which flowers remain under natural conditions and natural fruit set can be observed; (iv) manual self-pollination, in which flowers are pollinated with their own pollen, in order to investigate self-compatibility; (v) manual geitonogamy, which involves the pollen of a flower fertilizing another flower from the same parent plant or from a clone; (vi) manual cross-pollination, in which flowers are previously emasculated and then manually pollinated with the pollen from another individual; and (vii) natural cross-pollination, with emasculated flowers left under natural conditions [ 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 ]. Among these treatments, manual self-pollination and manual cross-pollination are usually more successful in fruit production and exhibit high fruit sets.…”

“…In another recent study, V. palmarum flowers exhibited nectar production and storage, and secretory cells longitudinally disposed in the labellum. This species’ flowers seem to be adapted to hummingbirds’ pollination [ 42 ]. According to Pansarin [ 32 ], the new findings regarding the pollinator attraction mechanism of Vanilla flowers suggest that the previous assumption of a reward absence is possibly due to a scarcity of information and the limited number of studied species.…”

“…In Brazil, recent records of V. palmarum indicated that flowers produce nectar and are pollinated by hummingbirds, but autogamy may also occur. The fruit set of Brazilian populations of V. palmarum was high in both natural (67.3–71.4%) and bagging (66.6–73.3%) experiment conditions [ 42 ]. In V. humblotii , despite the presence of a large rostellum covering the stigma surface and the pollinator dependence, unexplained spontaneous self-fertilization was reported, with 6.7% of fruit set [ 39 ], but the natural fruit set is low (~1%).…”

“…Although information regarding pollination and biological interactions of Vanilla are scarce [ 61 ] and natural pollination is still poorly understood [ 41 ], there have been recent efforts for their elucidation [ 32 , 35 , 36 , 37 , 39 , 40 , 41 , 42 , 49 , 51 , 53 ]. According to Childers and Cibes [ 55 ], hummingbirds and small Melipona bees were thought to be the pollinators of Vanilla in Mexico.…”

“…Visits by birds were also observed in V. planifolia flowers, which were occasionally visited by hummingbirds [ 29 ], and visits by the bird Zosterops were observed in vanilla plantations in Reunion Island [ 62 ]. In a recent study, Pansarin and Ferreira [ 42 ] observed a species of hummingbird ( Amazilia fimbriata ) pollinating V. palmarum flowers. The birds were observed hovering in front of the inflorescences, landing on the labellum apex, and placing their head inside the floral tube, which contained nectar in the nectar chamber.…”