Summary Mutualism between long corolla tubed plants and their potential pollinators, long‐tongued flies, is a classic example of coevolution, but to date, has only been reported from the regions of southern Africa. Many plant species from the Himalayas also show botanical characteristics that could be consistent with pollination by long‐tongued flies. Here, we seek the evidence of the “long‐tongued‐long tubed fly/flower” mutualism out of Africa, in a different continent and climatic region, the Himalayas.Floral traits of Himalayan region endemic alpine genus, Roscoea, indicate possible mutualism with long‐tongued flies for pollination success; however, effective pollinators of this genus are yet unknown. This study investigates whether long‐tongued flies and Roscoea purpurea in Nepal Himalayas show exclusive mutualism for their survival/reproduction.We made extensive observations of floral visitors of R. purpurea and food source of Philoliche longirostris across their wide ranges of populations in Nepal Himalayas for three consecutive years (2012–2014). To confirm the obligate reliance of R. purpurea upon P. longirostris for pollination success, manipulated pollination experiments were conducted at two populations for 2 years. Similarly foraging behavior, visitation frequency, and pollination efficiency of P. longirostris were assessed at two populations for 2 years, and its contribution for the reproductive success of R. purpurea was evaluated. Our results indicate that R. purpurea is self‐compatible but lacks autonomous selfing and obligatorily relies on P. longirostris for reproductive success. Across all populations, P. longirostris was observed as an exclusive and highly efficient pollinator of R. purpurea, while P. longirostris exclusively depends up on R. purpurea for food source.Out of Africa, this study provides the first evidence of long‐tongued fly pollination system and indicates the possibility of additional instances of such a rare phenomenon in the Himalayas. Finding of specialized pollinator of Roscoea only at its evolutionary center indicates that Roscoea species are originally pollinated by long‐tongued flies. Spatial mismatch with specialized pollinators may have induced the evolution of autonomous selfing in North Indochinese clades of Roscoea. This finding thus substantiates how geographic disjunction causes the shifting of pollination mechanism in closely related plant species.
Temporal flower closure is a non-morphological floral character of adaptive significance for growth of some species in extreme environments, and it has important implications for plant reproductive success. Flowers of Tulipa species responded to changes in temperature and closed temporarily at low temperatures, but they reopened when temperatures increased. In this study, we determined the effects of temporal flower closure of Tulipa iliensis Regel. on mating pattern, flower microenvironmental temperature, and sexual organ functions during exposure to low temperatures, rainfall, and wind. First, flowers of T. iliensis were incompletely herkogamous with stamens longer than the pistil. Floral closure resulted in the contact of dehisced anthers with the stigma and auto-pollen deposition on the stigma, thus facilitating automatic self-pollination. Second, floral closure maintained the temperature inside the flower, providing a stable microenvironment that promoted pollen germination and avoided a decline in stigma receptivity. Third, flower closure of T. iliensis before rainstorms avoided flushing of pollen from anthers and helped maintain both pollen viability and stigma receptivity during exposure to rain. Finally, flower closure maintained pollen clumping in the anthers during exposure to wind, thereby enhancing pollination efficiency by pollinators and/or automatic selfing. Therefore, temporal flower closure of T. iliensis is an important floral strategy in facilitating automatic selfing, extending the functional period of male and female organs, and it thus ensures reproductive success in the unpredictable early spring environment.
Floral sexual organ (stamen and pistil) movements are selective adaptations that have different functions in male-female reproduction and the evolution of flowering plants. However, the significance of stamen movements in the spatial–temporal function and separation of male and female organs has not been experimentally determined in species exhibiting floral temporal closure. The current study investigated the role of slow stamen (group-by-group) movement in male-female sexual function, and the effect of stamen movement on pollen removal, male-male and male-female interference, and mating patterns of Geranium pratense , a plant with temporal floral closure. This species uses stamen group-by-group movement and therefore anther-stigma spatial–temporal separation. Spatial separation (two whorls of stamen and pistil length) was shown to be stronger than temporal separation. We found that stamen movements to the center of the flower increase pollen removal, and the most common pollinators visited more frequently and for longer durations during the male floral stage than during the female floral stage. Petal movements increased both self-pollen deposition rate and sexual interference in G. pratense . The fruit and seed set of naturally and outcrossed pollinated flowers were more prolific than those of self-pollinated flowers. Group-by-group stamen movement, dehiscence of stamens, pistil movement, and male-female spatial–temporal functional separation of G. pratense before floral temporal closure may prevent male-female and stamen-stamen interference and pollen discounting, and may increase pollen removal and cross-pollination.
Plant populations at high elevation face extreme climatic conditions and resource limitations. The existence of distylous species at different elevations can help us investigate their adaptation to high altitudes, the evolution of their morphological characteristics, as well as their responses to limited resources. Here, 17 populations of Primula nivalis at different elevations were evaluated regarding variations in plant morphological characteristics, biomass allocation, and morphological plasticity in a heterogeneous environment. Our results demonstrate that heterogeneous environments can affect plant morphological characteristics and resource allocation in each sexual morph of these plants. Moreover, environmental variations reduced morphological plasticity in the two plant morphs, and the plasticity of long style (LS) plants was greater than that of short style (SS) plants. There were significant negative correlations between morphological characteristics and elevation, rainfall, temperature, and sunshine, and these are the main variables that affect morphological characteristics and resource allocation of both morphs of P. nivalis plants in heterogeneous environments. The morphological characteristics of P. nivalis plants transplanted from high to lower elevations were not significantly different in either population. LS plants had greater morphological plasticity and adaptability in heterogeneous environments than SS plants. Elevational gradients and heterogeneous environments differentiated both morphs of P. nivalis plants with regards to morphology as well as adaptations. LS plants showed a higher level of adaptability than SS plants.
Pollinator shift and its influence on floral traits have been well documented to explain the diversity of angiosperms, but such effects are still less known at the intraspecific level, especially the responses of different morphs of distylous plants. We hypothesized that the pollen transfer efficiency would decrease if the pollinator shifted from a long-tongued to short-tongued insect across populations, and plants would evolve towards selfing in response to the stressed pollination environment. Given the gender specialization between flower morphs, the long styled (L-morph) plants would increase female reproduction. Our study showed that the short-tongued Bombus tianshanicus, the most-visit pollinator in high elevation populations of distylous Primula nivalis, was less efficient in pollen transfer than long-tongued Bombylius major. The plants evolved to promote selfing through reducing the anther-stigma separation and increasing intramorph self-compatibility. The hand pollination experiment showed that after intramorph selfing, the fruit set and seed set increased with increasing elevation. Moreover, anther and stigma were closer in the L-morph than in the short styled (S-morph) plants, and the L-morphs showed higher pollen transfer efficiency than the S-morphs. Along with increased self-compatibility, the fruit set and seed set of L-morph plants were significantly higher than those of S-morph plants. We described the pollinator shifts along an elevation gradient in a distylous plant and the response of plants by promoting selfing, which confirmed our hypothesis and supported the pollinator-shift model. Our study also highlighted the different response in self-compatibility between flower morphs.
Environmental conditions are likely to cause some of the variation in sexual expression found in .. Both genetic and ecological factors likely contribute to the maintenance of sexual variation in this species.
The population characteristics of distylous species are highly sensitive to stochastic natural selection pressure. Therefore, populations growing under different environmental conditions may vary in floral morph ratios, potentially affecting female fitness and leading to inbreeding depression. However, the variation in offspring quality among populations as a result of inbreeding depression is poorly understood in distylous species. This study investigates variations in plant density, seed mass, seed viability, female fitness, and post-dispersal inbreeding depression in both sexual morphs (long-styled and short-styled plants) of the distylous Primula nivalis that were subjected to different pollination treatments along an elevational gradient from 1657 to 2704 m a.s.l. Population characteristics (morph plant density and ratio) and fruit set were significantly affected by sexual morph and elevation. Plant density and fruit set frequencies were lower for short-styled than for long-styled plants at 2704 m a.s.l. The seeds from the cross-pollinated flowers of both morphs were higher in quality than those of self-pollinated flowers. The female fitness of seeds from cross-pollinated flowers of both morphs was higher than that of seeds from open-pollinated and self-pollinated flowers. The female fitness of seeds from long-styled flowers was higher than that of seeds from short-styled flowers at all elevations. Inbreeding depression increased with elevation among plants with short-styled flowers but not among those with long-styled flowers. Variation in the elevation-dependent mating system might influence female fitness and affect inbreeding depression in both floral morphs. In conclusion, the low quality of seeds from short-styled flowers at high elevations might decrease short-styled flower frequency, affecting population characteristics.
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