Data from: Heterostyly promotes disassortative pollination and reduces sexual interference in Darwin’s primroses: evidence from experimental studies

Different strategies to reduce selfing and promote outcrossing have evolved in hermaphroditic flowers. Heterostyly, a complex floral polymorphism that occurs in at least 27 families of angiosperms, is hypothesized to achieve both goals by optimizing cross-pollination (via disassortative pollen transfer) and restricting gamete wastage to autogamy (via the reduction of sexual interference between male and female organs). In heterostylous flowers, the reciprocal positioning of sexual organs in different morphs and the pollen incompatibility-system within flower or between flowers of the same morph are thought to optimize both male and female functions, reducing the conflicts inherent to the occurrence of both sexual organs in the same reproductive unit. Specific elements of the disassortative-pollination and sexual-interference hypotheses have been tested individually before. However, despite the long-standing interest in heterostyly – ever since Darwin's seminal work on primroses – the predictions derived from these two hypotheses have never been experimentally and systematically examined in the same system. Using distylous primroses (Primula elatior, P. vulgaris) we compare pollen transfer (i) between reciprocal and non-reciprocal flowers; (ii) from anthers onto different parts of the pollinator's body; (iii) within flower and between flowers of the same morph. We further test whether (iv) anther-stigma distance correlates with self-pollen transfer; (v) seed-set differs after pollinations with compatible, incompatible, and both pollen types. Reciprocal herkogamy promotes differential placement of pollen onto different parts of the pollinator's body, thus effecting transfer of more pollen to reciprocal than non-reciprocal stigmas and realizing the key predictions of the disassortative-pollination hypothesis. However, short-styled flowers transfer pollen more disassortatively than long-styled flowers in both species, whereas long-styled flowers export more pollen to non-reciprocal than reciprocal stigmas in P. vulgaris, thus compromising male function in this species. Furthermore, larger distance between sexual organs lowers self- and intra-morph pollination and the pollen incompatibility-system decreases seed production after self-pollination, thus diminishing sexual interference. Our results help us understand how the morphological and physiological components of heterostyly contribute to optimizing pollen transfer and minimizing self- and intra-morph pollination, thus promoting more efficient outcrossing in species with this floral polymorphism.

雌雄同花植物演化出多种策略以减少自交、促进异交。花柱异长（heterostyly）是一种复杂的花部多态现象，目前已知至少存在于27个被子植物科中，学界推测其可通过优化异花授粉（借助异配花粉传递）以及降低雌雄器官间的性干扰以限制自交导致的配子浪费，从而同时达成上述两个目标。在花柱异长的花部结构中，不同花型的性器官呈交互排布，且同朵花或同型花之间存在花粉不亲和系统（pollen incompatibility-system），这些特征被认为可优化雌雄生殖功能，缓解同一繁殖单元同时具备两种性器官所固有的冲突。此前，异配花粉传递与性干扰假说的特定论点已被分别验证。然而，尽管自达尔文对报春花的开创性研究以来，学界对花柱异长的关注由来已久，但这两个假说衍生的预测却从未在同一系统中得到系统性的实验验证。本研究以二型花柱（distylous）的报春花属植物（Primula elatior、P. vulgaris）为研究对象，比较三类花粉传递情况：（i）交互花型与非交互花型之间的花粉传递；（ii）花粉从花药到传粉者身体不同部位的附着分布；（iii）同朵花内以及同型花之间的花粉传递；此外，本研究还进一步检验了两项预测：（iv）雌雄器官间距与自花花粉传递是否存在相关性；（v）采用亲和、不亲和以及混合花粉授粉后的结实率差异。研究结果显示，交互雌雄异位可促进花粉在传粉者身体不同部位的差异化附着，从而使更多花粉传递至交互花型的柱头上，而非非交互花型，这验证了异配花粉传递假说的核心预测。不过，在两个物种中，短花柱花型的异配花粉传递效率均高于长花柱花型；而在普通报春（P. vulgaris）中，长花柱花型向非交互花型传递的花粉量反而多于交互花型，这会削弱该物种的雄性生殖功能。此外，雌雄器官间距越大，自花与同型花粉传递量越低；花粉不亲和系统则会降低自花授粉后的结实率，从而缓解性干扰。本研究结果有助于我们理解花柱异长的形态与生理组分如何协同优化花粉传递、减少自花与同型花粉传递，进而在具备该花部多态现象的物种中实现更高效的异交。