A putative nursery pollination mutualism between Japanese Chrysosplenium plants and Nipponorhynchus sawflies

Abstract

Societal Impact Statement Understanding ecological interactions is increasingly important for biodiversity conservation. This study reveals a unique nursery pollination mutualism between Japanese endemic plants and sawflies. These partners exhibit tightly synchronized life cycles in riparian forests, making them sensitive to environmental changes. Importantly, our results reveal fine‐scale geographic variation in floral morphology, proboscis length, and interaction strength, suggesting that local populations maintain distinct ecological and evolutionary patterns. These findings indicate that conservation strategies should consider not only species‐level protection but also the maintenance of local interaction networks, ensuring the stability of these fragile, specialized ecological interactions and the diversity of both partners. Summary Nursery pollination mutualisms—where insects act as pollinators but their larvae consume developing seeds—provide significant insight into how reciprocal selection drives specialization and diversification. The Chrysosplenium ser. Macrostemon (Saxifragaceae) exhibits remarkable floral diversity with an unclear evolutionary trajectory. We hypothesized this group engages in nursery pollination mutualism with Nipponorhynchus sawflies (Hymenoptera: Tenthredinidae), potentially explaining their floral divergence. We surveyed floral visitors in 29 populations and larval parasitism in 10 populations and conducted pollinator exclusion experiments in six populations to evaluate pollinator dependence. Pollen loads were examined on 154 Nipponorhynchus specimens. Proboscis length of Nipponorhynchus was measured to evaluate geographic variation and morphological adaptation to host floral types. Nipponorhynchus bimaculatus and Nipponorhynchus mirabilis were the dominant pollinators of most Macrostemon taxa. Adult sawflies exclusively visited Macrostemon flowers, carrying abundant pollen. Larvae were found only in fruits of Macrostemon species, indicating strict host specificity. Pollinator exclusion significantly reduced fruit set, demonstrating a fitness benefit of visitation, although autonomous self‐pollination provided baseline reproductive assurance. Furthermore, both sawfly species exhibited marked geographic variation in proboscis length, independent of body size, consistent with possible adaptation to local floral morphologies. Our findings reveal a putative new case of nursery pollination mutualism between Macrostemon plants and Nipponorhynchus sawflies—the first case involving sawflies. This system provides a valuable model for understanding how fine‐scale reciprocal selection can drive coordinated morphological diversification in both partners across populations with varying mutual dependence.