Adaptive radiations occur mostly in response to environmental variation through the evolution of key innovations that allow emerging species to occupy new ecological niches. Such biological innovations may play a major role in niche divergence when emerging species are engaged in reciprocal ecological interactions. To demonstrate coevolution is a difficult task; only a few studies have confirmed coevolution as driver of speciation and diversification. Herein we review current knowledge about bee orchid (Ophrys spp.) reproductive biology. We propose that the adaptive radiation of the Mediterranean orchid genus Ophrys, comprising several hundred species, is due to coevolutionary dynamics between these plants and their pollinators. We suggest that pollination by sexual swindling used by Ophrys orchids is the main driver of this coevolution. Flowers of each Ophrys species mimic a sexually receptive female of one particular insect species, mainly bees. Male bees are first attracted by pseudo‐pheromones emitted by Ophrys flowers that are similar to the sexual pheromones of their females. Males then are lured by the flower shape, colour and hairiness, and attempt to copulate with the flower, which glues pollen onto their bodies. Pollen is later transferred to the stigma of another flower of the same Ophrys species during similar copulation attempts. In contrast to rewarding pollination strategies, Ophrys pollinators appear to be parasitized. Here we propose that this apparent parasitism is in fact a coevolutionary relationship between Ophrys and their pollinators. For plants, pollination by sexual swindling could ensure pollination efficiency and specificity, and gene flow among populations. For pollinators, pollination by sexual swindling could allow habitat matching and inbreeding avoidance. Pollinators might use the pseudo‐pheromones emitted by Ophrys to locate suitable habitats from a distance within complex landscapes. In small populations, male pollinators would disperse once they have memorized the local diversity of sexual pseudo‐pheromone bouquets or if all Ophrys flowers are fertilized and thus repel pollinators via production of repulsive pheromones that mimic those produced by fertilized female bees. We propose the following evolutionary scenario: Ophrys radiation is driven by strong intra‐specific competition among Ophrys individuals for the attraction of species‐specific pollinators, which is a consequence of the high cognitive abilities of pollinators. Male bees record the pheromone signatures of kin or of previously courted partners to avoid further copulation attempts, thereby inducing strong selection on Ophrys for variation in odour bouquets emitted by individual flowers. The resulting odour bouquets could by chance correspond to pseudo‐pheromones of the females of another bee species, and thus attract a new pollinator. If such pollinator shifts occur simultaneously in several indivuals, pollen exchanges might occur and initiate speciation. To reinforce the attraction of the new pollinator and secure prezygotic isolation, the following step is directional selection on flower phenotypes (shape, colour and hairiness) towards a better match with the body of the pollinator's female. Pollinator shift and the resulting prezygotic isolation is adaptive for new Ophrys species because they may benefit from competitor‐free space for limited pollinators. We end our review by proritizing several critical research avenues.

中文翻译：

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为什么有这么多蜂兰花品种？通过种内竞争对传粉媒介的适应性辐射

适应性辐射主要是通过允许新兴物种占据新生态位的关键创新的进化来响应环境变化。当新兴物种参与互惠生态相互作用时，这种生物创新可能在生态位分化中发挥重要作用。证明协同进化是一项艰巨的任务；只有少数研究证实共同进化是物种形成和多样化的驱动因素。在此，我们回顾了有关蜂兰花 (Ophrys spp.) 生殖生物学的当前知识。我们提出地中海兰花属 Ophrys 的适应性辐射，包括数百种，是由于这些植物与其授粉者之间的共同进化动力学。我们认为 Ophrys 兰花使用的性欺骗授粉是这种共同进化的主要驱动力。每个 Ophrys 物种的花模仿一种特定昆虫物种的性接受雌性，主要是蜜蜂。雄蜂首先被 Ophrys 花释放的伪信息素所吸引，这些伪信息素与雌蜂的性信息素相似。然后雄性被花的形状、颜色和毛羽所吸引，并试图与花交配，花将花粉粘在它们的身上。在类似的交配尝试中，花粉后来转移到同一 Ophrys 物种的另一朵花的柱头上。与奖励授粉策略相反，Ophrys 授粉者似乎被寄生了。在这里，我们提出这种明显的寄生现象实际上是 Ophrys 与其传粉者之间的共同进化关系。对植物来说，通过有性欺骗授粉可以保证授粉效率和特异性，以及种群间的基因流动。对于传粉者来说，通过性欺骗授粉可以实现栖息地匹配和近亲繁殖的避免。传粉者可能会使用 Ophrys 发出的伪信息素在复杂的景观中从远处定位合适的栖息地。在小种群中，雄性传粉者一旦记住了有性假信息素花束的局部多样性，或者如果所有 Ophrys 花都受精，从而通过产生与受精雌性蜜蜂产生的相似的排斥性信息素来排斥传粉者，雄性传粉者就会分散。我们提出以下进化方案：Ophrys 辐射是由 Ophrys 个体之间强烈的种内竞争驱动的，以吸引物种特异性传粉者，这是传粉者高认知能力的结果。雄性蜜蜂会记录亲属或先前求偶伴侣的信息素特征，以避免进一步的交配尝试，从而诱导对 Ophrys 的强烈选择，以了解个别花朵散发出的气味花束的变化。由此产生的气味花束可能与另一种蜜蜂雌性的伪信息素相对应，从而吸引新的传粉者。如果这种传粉媒介转变同时发生在几个个体中，则可能发生花粉交换并引发物种形成。为了加强对新传粉者的吸引力并确保合子前隔离，接下来的步骤是对花表型（形状、颜色和毛羽）进行定向选择，以便与传粉者雌性的身体更好地匹配。传粉媒介转移和由此产生的合子前隔离适用于新的 Ophrys 物种，因为它们可能受益于有限传粉媒介的无竞争空间。我们通过优先考虑几个关键研究途径来结束我们的审查。