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.雌雄同花植物中演化出多种降低自交、促进异交的策略。花柱异型（heterostyly）是一种复杂的花部多态现象，目前至少在27个被子植物（angiosperms）科中被发现，学界推测其可通过优化异花授粉（借助异型花粉传递（disassortative pollen transfer））并限制自交造成的配子浪费（通过减少雌雄器官间的性干扰），同时实现上述两个目标。在花柱异型花中，不同花型的性器官交互排布，以及同型花内或同型花间的花粉不亲和系统（pollen incompatibility-system），被认为可优化雌雄生殖功能，缓解同一生殖单元同时具备两种性器官所固有的演化冲突。此前，异型花粉传递与性干扰这两个假说的具体内容已分别得到检验。然而，尽管自达尔文对报春花的开创性研究以来，学界长期关注花柱异型，但这两个假说衍生出的预测，从未在同一研究系统中得到系统性的实验验证。本研究以二型花柱的报春花属植物——高报春（Primula elatior）与普通报春（Primula vulgaris）为实验材料，对比花粉传递的以下特征：(i) 交互型与非交互型花之间的花粉传递；(ii) 花药向传粉者身体不同部位的花粉附着；(iii) 同花内及同型花间的花粉传递；此外，我们还检验了：(iv) 花药-柱头间距是否与自花花粉传递量相关；(v) 采用亲和、不亲和以及混合花粉授粉后，结籽率是否存在差异。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，从而使异型花柱头获得的花粉量多于非异型花，验证了异型花粉传递假说的核心预测。但在两个物种中，短花柱花的异型花粉传递效率均高于长花柱花；而在普通报春中，长花柱花向非异型柱头传递的花粉量多于异型柱头，进而削弱了该物种的雄性生殖功能。此外，雌雄器官间距越大，自花及同型花间的授粉量越低；花粉不亲和系统则会降低自花授粉后的结籽率，从而减轻性干扰。本研究结果有助于理解花柱异型的形态与生理组分如何通过优化花粉传递、减少自花及同型花间的授粉，从而在具备该花部多态现象的物种中促进更高效的异交。