Pollination niche availability facilitates colonization of Guettarda speciosa with heteromorphic self-incompatibility on oceanic islands

Abstract

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.

Figure 1

Floral morphology of Guettarda speciosa, showing the position of anther and stigma, and measurements of floral characters. CoD: corolla diameter; CoTL: corolla tube length; CoTD: corolla tube diameter; SCoS: stigma-corolla separation; SAS: stigma-anther separation; AH: anther height; SH: stigma height; CoAS: corolla-anther separation; SD&L: stigma’s diameter and length. Bar = 10 mm.

Figure 2

Guettarda speciosa pollen tube growth in vivo after hand pollination. (A) L-morph style 24 h after inter-morph pollination; (B) L-morph style 24 h after self-pollination; (C) S-morph style 24 h after self-pollination; (D) S-morph style 24 h after inter-morph pollination. Bar = 1 mm.

Figure 3

The flower and pollinator of Guettarda speciosa in study site. (A) Blooming inflorescence shows narrow corolla throat; (B) Agrius convolvuli is pollinating the flowers; (C) length comparison of the tongue of A. convolvuli and corolla tube of G. speciosa. Bar = 10 mm. (D) Ipomoea pes-caprae in natural habitat; (E) larva of A. convolvuli feeding on the leaves of I. pes-caprae, the host plant.

Figure 4

ENM predicted distribution regions of Guettarda speciosa (A), Agrius convolvuli (B) and Ipomoea pes-caprae (C).

Figure 5

ENM predicted distribution regions for Guettarda speciosa (green), Agrius convolvuli (yellow) and Ipomoea pes-caprae (blue) in 10th percentile training presence. Red color highlights the overlapping areas of the three species, and black dots indicate the occurrence records of G. speciosa. Figures B and C illustrate the details of the regions in the dashed boxes in figure A. Red dashed circle in figure C highlights the experimental site, Yongxing Island.

Figure 6

Suitable range for Agrius convolvuli (Red), Guettarda speciosa (Blue), overlapping regions (Yellow) in 10^th percentile training presence.