Pollinator sharing and hybridization in a pair of dioecious figs sheds light on the pathways to speciation----Xishuangbanna Tropical Botanical Garden,CAS

First Author:

Huang, Jian-Feng

Abstract:

The dynamics and processes underlying the codiversification of plant-pollinator interactions are of great interest to researchers of biodiversity and evolution. Cospeciation is generally considered a key process driving the diversity of figs and their pollinating wasps. Groups of closely related figs pollinated by separate wasps occur frequently and represent excellent opportunities to study ongoing diversification in this textbook mutualism. We study two closely related sympatric dioecious figs (Ficus heterostyla and Ficus squamosa) in Xishuangbanna, southwest China, and aim to document what is likely to be the final stages of speciation between these species using a combination of trait data and experimental manipulation. Volatile profiles at the receptive phase, crucial for attracting pollinators, were analyzed. In total, 37 and 29 volatile compounds were identified from receptive F. heterostyla and F. squamosa figs, respectively. Despite significant interspecific dissimilarity, 25 compounds were shared. Ovipositor lengths lie well within range required for access to heterospecific ovules, facilitating hybridization. Cross introduction of wasps into figs was conducted and hybrid seeds were generated for all donor/recipient combinations. F. heterostyla wasps produce adult offspring in F. squamosa figs. While F. squamosa wasps induce gall development in F. heterostyla figs and their offspring fail to mature in synchrony with their novel host. We record limited geographic barriers, minimal volatile dissimilarity, compatible morphology, complementary reproductive phenologies, and the production of hybrid seeds and wasp offspring. These findings suggest ongoing wasp specialization and reproductive isolation, potentially applicable to other related fig species. The coevolution of flowering plants and their animal pollinators is essential for fostering biodiversity. Exploring the dynamics and processes underlying plant-pollinator interactions is of evolutionary interest and critical for understanding biodiversity origins. Ficus, a diverse genus, is well-known for its species-specific relationships with pollinating wasps. Cospeciation plays an important role in the formation of fig and wasp diversity, as the reciprocal adaptations have led to the development of strong prezygotic barriers. Nevertheless, wasps exhibit much shorter generation times compared to figs, resulting in faster speciation rates. Often, fig complexes or closely related figs coevolve with distinct wasp species, representing the final step toward complete fig speciation and providing an excellent opportunity for studying ongoing mutualistic diversification. In such scenarios, heterospecific visitation of wasps may trigger interspecific pollination. Here, we examined reproductive isolation between two closely related figs, Ficus heterostyla and Ficus squamosa, through trait data and experimental manipulation. Floral volatiles emitted by receptive figs, which are crucial signals for attracting specific wasps, exhibited considerable overlap between these two fig species. The lengths of the wasp ovipositors were well within the range required for access to heterospecific ovules. Hybrid seeds were produced experimentally, with results showing that wasps of F. heterostyla reproduced in F. squamosa figs, while wasps of F. squamosa did not reproduce in F. heterostyla figs. Overall, heterospecific visitation decreased both fig and wasp fitness. Together with geographic barriers and complementary reproductive phenologies, these findings suggest that prezygotic isolation between F. heterostyla and F. squamosa may not yet be established.

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Wang, B

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2023

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EVOLUTION LETTERS

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