Evolution of pollination and breeding systems of Antillean Gesneriaceae

Abstract

Islands serve as one of our most important model systems for understanding the role of the environment on character evolution and diversification. This study examined the role of pollinators on the evolution of floral traits and breeding system on the tribe Gesnerieae (Gesneriaceae), a monophyletic radiation from the Antilles that encompasses great floral diversity. Pollinator observations were conducted over 5 years (2003-2007) for 19 species of Gesnerieae across multiple islands. Pollination systems include specialized systems (i.e. one functional group of floral visitors, e.g. hummingbird or bats) and generalized systems (e.g. various functional groups, e.g., bats, birds and insects). Hummingbird-pollinated species have the lowest frequencies of pollinator visitation (mean number of visits per flower/ per day =1 ± 1.5 SE) compared to bat-pollinated (mean= 2 ± 1.8) and generalist species (mean=13 ± 1.8). A multivariate analysis of floral traits provides strong support for correlated sets of floral traits associated with bat and hummingbird pollination supporting the pollination syndrome concept (the notion that flowers evolve integrated phenotypes in response to selection by the most important pollinators). A two-year pollen limitation study of nine species was conducted to evaluate how differences in visitation among different pollination system influenced plant female reproductive success; this study resulted in significant pollen limitation for specialized species with low visitation only (bat and hummingbird-pollinated). Furthermore, emasculation experiments demonstrated that ornithophilous species use autonomous self-pollination as a reproductive assurance mechanism. A survey of potential autonomous self-pollination for 15 Gesnerieae representative of all floral phenotypes supported an association between this breeding system hummingbird-pollinated tubular-flowered species. Last, phylogenetic analyses of two nuclear DNA regions (ITS and GCYC) and a morphological data set revealed that bat and generalized pollination evolved from hummingbird pollination. Furthermore, autonomous self-pollination originates only in ornithophilous lineages of Gesnerieae. Overall these results provide evidence for the evolution of generalization and autonomous breeding systems, as two alternative reproductive strategies in response to inadequate hummingbird pollination service in insular ecosystems. This study underscores the utility integrating the study of pollination and breeding systems within a phylogenetic context to provide further insights into the ecological conditions that can influence floral evolution.