Obligate out-breeding plants are considered relatively disadvantageous comparing with self-breeding plants when colonizing oceanic islets following long-distance dispersal owing to mate and pollinator limitation. The rarity of heterostyly, a typical out-breeding system, on oceanic islands seems a good proof. However, a heterostylous plant, Guettarda speciosa, is widely distributed on most tropical oceanic islets. Our research demonstrates that its heteromorphic self-incompatibility, plus herkogamy and long flower tube make it rely on pollinator for sexual reproduction, which is generally considered “disadvantageous” for island colonization. We hypothesize that available pollination niche will be a key factor for its colonization on islands. Our studies on remote coral islands show that G. speciosa has built equilibrium population with a 1:1 morph ratio. It could obtain pollination niche from the hawkmoth Agrius convolvuli. A pioneer island plant Ipomoea pes-caprae sustain the pollination niche by providing trophic resource for the larvae of the pollinator. Geographic pattern drawn by Ecological Niche Modelling further indicates the interaction between G. speciosa, A. convolvuli and I. pes-caprae can be bounded on those remote oceanic islands, explaining the colonization of G. speciosa distylous population. These findings demonstrated obligate out-breeding system could be maintained to acclimatize long distance dispersal, if the pollination niche is available.

Background: The evolution of heterostyly, a genetically controlled floral polymorphism, has been a hotspot of research since the 19th century. In recent years, studies on the molecular mechanism of distyly (the most common form of heterostyly) revealed an evolutionary convergence in genes for brassinosteroids (BR) degradation in different angiosperm groups. This floral polymorphism often exhibits considerable variability that some taxa have significant stylar dimorphism, but anther height differs less. This phenomenon has been termed “anomalous” distyly, which is usually regarded as a transitional stage in evolution. Compared to “typical” distyly, the genetic regulation of “anomalous” distyly is almost unknown, leaving a big gap in our understanding of this special floral adaptation strategy.Methods: Here we performed the first molecular-level study focusing on this floral polymorphism in Guettarda speciosa (Rubiaceae), a tropical tree with “anomalous” distyly. Comprehensive transcriptomic profiling was conducted to examine which genes and metabolic pathways were involved in the genetic control of style dimorphism and if they exhibit similar convergence with “typical” distylous species.Results: “Brassinosteroid homeostasis” and “plant hormone signal transduction” was the most significantly enriched GO term and KEGG pathway in the comparisons between L- and S-morph styles, respectively. Interestingly, homologs of all the reported S-locus genes either showed very similar expressions between L- and S-morph styles or no hits were found in G. speciosa. BKI1, a negative regulator of brassinosteroid signaling directly repressing BRI1 signal transduction, was identified as a potential gene regulating style length, which significantly up-regulated in the styles of S-morph.Discussion: These findings supported the hypothesis that style length in G. speciosa was regulated through a BR-related signaling network in which BKI1 may be one key gene. Our data suggested, in species with “anomalous” distyly, style length was regulated by gene differential expressions, instead of the “hemizygous” S-locus genes in “typical” distylous flowers such as Primula and Gelsemium, representing an “intermediate” stage in the evolution of distyly. Genome-level analysis and functional studies in more species with “typical” and “anomalous” distyly would further decipher this “most complex marriage arrangement” in angiosperms and improve our knowledge of floral evolution.