Why are there so many bee‐orchid species? Adaptive radiation by intra‐specific competition for mnesic pollinators

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.