Covariation in reproductive investment between sterile and fertile sex organs contributes to sterile stamens persistence in cryptically dioecious Actinidia

不育和可育性器官之间生殖投入的协同变化导致了隐性雌雄异株猕猴桃属植物中不育雄蕊的持续存在。

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Abstract

BACKGROUND: Cryptic dioecy is a sexual system in which individuals of at least one sex are morphologically hermaphroditic but functionally unisexual. The presence of non-functional reproductive organs may represent an intermediate stage during the evolutionary transition from hermaphroditism to dioecy. The ancestral hypothesis suggests that sterile sex organs may persist as vestiges of an ancestral bisexual state, potentially due to their low resource cost or absence of significant conflict with fertile organs, yet this has rarely been tested. All Actinidia species exhibit cryptic dioecy with morphological androdioecy, providing an ideal system for testing this hypothesis. METHODS: This study investigated floral traits and biomass allocation of floral organs across nine Actinidia taxa, and used phylogenetic independent contrasts (PIC) across 28 taxa to examine correlations among floral traits. The aims were to reveal the resource investment in sterile sex organs and their relationships with other floral structures, and to test the ancestral hypothesis. RESULTS: Although functionally female flowers of Actinidia are morphologically perfect, their pollen grains are sterile. Stamen number exhibited high interspecific variation in both floral morphs. The biomass allocation proportion to sterile stamens in functionally female flowers was significantly lower compared to that allocated to fertile stamens in male flowers. Furthermore, significantly positive correlations were observed between sterile and fertile sex organs across multiple traits in functionally female flowers, at both species and genus levels. CONCLUSIONS: These results suggest that floral traits in Actinidia have evolved into a highly integrated modular structure. Sterile stamens in functionally female flowers have low resource costs and exhibit a synergistic effect during development or resource allocation with female organs. This study provides support for the ancestral hypothesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-025-08035-y.

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