Maintenance of specificity in sympatric host-specific fig/wasp pollination mutualisms

Abstract

Background: Fig/wasp pollination mutualisms are extreme examples of species-specific plant-insect symbioses, but incomplete specificity occurs, with potentially important evolutionary consequences. Why pollinators enter alternative hosts, and the fates of pollinators and the figs they enter, are unknown.

Methods: We studied the pollinating fig wasp, Ceratosolen emarginatus, which concurrently interacts with its typical host Ficus auriculata and the locally sympatric alternative host F. hainanensis, recording frequencies of the wasp in figs of the alternative hosts. We measured ovipositor lengths of pollinators and style lengths in female and male figs in the two host species. Volatile organic compounds (VOCs) emitted by receptive figs of each species were identified using GC-MS. We tested the attraction of wasps to floral scents in choice experiments, and detected electrophysiologically active compounds by GC-EAD. We introduced C. emarginatus foundresses into figs of both species to reveal the consequences of entry into the alternative host.

Results: C. emarginatus entered a low proportion of figs of the alternative host, and produced offspring in a small proportion of them. Despite differences in the VOC profiles of the two fig species, they included shared semiochemicals. Although C. emarginatus females prefer receptive figs of F. auriculata, they are also attracted to those of F. hainanensis. C. emarginatus that entered male figs of F. hainanensis produced offspring, as their ovipositors were long enough to reach the bottom of the style; however, broods were larger and offspring smaller than in the typical host. Female figs of F. hainanensis failed to produce seeds when visited by C. emarginatus. These findings advance our current understanding of how these species-specific mutualisms usually remain stable and the conditions that allow their diversification.

Keywords: Electrophysiology; Ficus; Fig wasps; Non-typical host-use; Species-specificity; Volatile organic compounds.

Figure 1. Illustration of sharing the pollinator between two distinct host Ficus species.

Figure 2. Characteristics of Ceratosolen emarginatus and Ceratosolen sp.

(A) Dorsal side of head of C. emarginatus; (B) ventral side of head of C. emarginatus; (C) dorsal side of head of Ceratosolen sp.; (D) ventral side of head of Ceratosolen sp.; (E) dorsal side of hind leg of C. emarginatus; (F) ventral side of hind leg of C. emarginatus; (G) dorsal side of hind leg of Ceratosolen sp.; (H) ventral side of hind leg of Ceratosolen sp. Scale: 200 µm. Note that, when the mandibulae are closed, the appendages of the female mandibulae are close to the maxilla in C. emarginatus while the mandibular appendages are more divergent from each other and hence more separated from the maxilla in Ceratosolen sp. Furthermore, the hind legs of C. emarginatus have a large ventral tooth in the coxa and a sharp tooth in the femur, thus differing from those of Ceratosolen sp.

Figure 3. Bioassays of female Ceratosolen emarginatus responses to receptive figs of Ficus auriculata and F. hainanensis performed using Y-tube olfactometer tests.

Figure 4. Non-metric multi-dimensional scaling of the relative proportions of VOCs emitted by receptive figs of Ficus auriculata and F. hainanensis based on Bray–Curtis dissimilarity index (stress = 0.062).

The tendency for a slight difference in receptive fig odour between sexes is non-significant whereas the difference between species is significant.

Figure 5. Electroantennographic responses of Ceratosolen emarginatus to receptive fig scent extracts of (A) Ficus auriculata and (B) F. hainanensis.

GC-FID (black line), and GC-EAD responses of C. emarginatus antennae (inverted blue line). VOC identification: 1: 2-Heptanone; 2: Ylangene; 3 and 1′: α-Copaene; 4: α-Funebrene; 5: α-Gurgujene; 6 and 3′: β-Funebrene; 7: trans- β-Farnesene; 8: α-Patchoulene; 9: β-Cadinene; 2′: α-Cedrene; 4′: β-Cedrene; 5′: α-Guaiaene; 6′: Aromadendrene).

Figure 6. The distribution of fig style length and ovipositor length of Ceratosolen emarginatus.

(A) Style length of receptive figs from Ficus auriculata; (B) Style length of receptive figs from F. hainanensis.