Reproductive strategies of animal‐pollinated plants on high mountains: A review of studies from the “Third Pole”

Abstract

Having hundreds of big mountains, the Qinghai–Tibetan Plateau and its southern boundary, the Hengduan Mountains Region, represent one of the world's biodiversity hotspots. In the so‐called “Third Pole of the earth”, diverse effects of climate change and habitat heterogeneity could have driven the evolution of plant adaptive strategies. In this review, we collected and compiled recent sources of reproductive biology in animal‐pollinated plants, stressing the questions that need further attention, including pollination system, pollen limitation, self‐compatibility, and sexual system. We constructed plant–pollinator interaction networks based on the case studies from this region, showing that the majority of pollinators were bees, moths, butterflies, and flies were also important, and bats and birds were rare. As the unpredictable (cold, rainy or windy) weather affects pollinator activities, sexual reproduction seemed to be pollen limited, but available studies show that the exact pattern of pollen limitation is still under debate. Self‐compatibility could be either a solution, or a result from pollen limitation. Moreover, plant sexual systems can be regarded as an integrated module that counters pollen limitation. As phylogenetic relationships were constructed, diverse genera experienced rapid radiation were revealed in these mountainous areas. Further studies of evolutionary transitions in reproductive systems of congeners will unveil potential factors shaping the general pattern of adaptive strategies in animal‐pollinated plants. Further studies will be beneficial in using advanced new techniques, examining phenotypic selection under common gardens, and considering chemical ecology in interactions between plants and florivores, particularly in pollen fate.

Altitude‐related shift of relative abundance from insect to sunbird pollination in Elaeagnus umbellata (Elaeagnaceae)

“…A recent study in Claytonia virginica L. found that, in populations where a pollen‐collecting bee dominated, plants produced relatively more pollen per flower and anther dehiscence was more staggered than plants in populations where a nectar‐collecting bee‐fly dominated, indicating an effect of pollinator foraging behavior on divergent pollen traits (Parker et al, 2018). Study of the selective landscape that drives shifts in pollination ecotypes remains one of the most important areas for understanding pollinator‐mediated floral evolution (Tong et al, 2021).…”

“…Sunbirds have been observed to be effective pollinators in winter‐flowering species and in high mountain regions (Cruden, 1972; Stiles, 1978) and plants in the eastern Himalayas (Davidar, 1983; Zhang et al, 2012; Huang et al, 2017). As bumblebees and flies are important pollinators for many flowering plants in the high mountains of the Hengduan region (Fang & Huang, 2016; Tong et al, 2021), we could expect a shift to sunbird pollination, providing plants with high pollination efficiency per visit but relatively low visit frequency. We observed that pollen limitation of seed production was more severe at high altitude in E. umbellata .…”

“…The ecotype has been widely recognized in natural, experimental, and agricultural plants (Wang et al, 2021). However, there is still little evidence for pollination ecotypes linked to altitude, where changes in floral traits associated with changes in pollinators among populations of a plant species are linked to altitudinal differences (Tong et al, 2021). Our field study on flowers of Elaeagnus umbellata Thunb.…”

Plant diversity and ecology on the Qinghai–Tibet Plateau

“…The authors also summarized genomic advancements related to high‐altitude adaptation of both plants and animals. Tong et al (2021) reviewed the reproductive strategies of animal‐pollinated alpine plants on the QTP, involving pollination system, pollen limitation, self‐pollination, and sexual system. In this region, 95.4% of animal‐pollinated plants are pollinated by insects (i.e., bees, moths, butterflies, and flies) with only 4% by vertebrates (i.e., bats and birds).…”

The mating system and reproductive assurance of <i>Rorippa elata</i> (Brassicaceae) across latitude

“…高山生物区(alpine biome)是唯一在全球广泛分 布的生物区, 也是地球上极端环境分布最集中和受 气 候 变 化 威 胁 最 严 重 的地 区 之 一 (Körner, 2020; Testolin et al, 2020;Wang T et al, 2021)。高山植物 (alpine plant)是地理分布中心位于高山生物区的植 物总称(Körner, 2003)。在长期极端环境的选择压力 下, 高山植物进化出了多样的适应性策略 Sun et al, 2014), 尤其是在繁殖方面 (彭德 力等, 2012;Barrett, 2014;Barrett & Harder, 2017;Tong et al, 2020)。 比 如 , 在传粉者稀缺时, 植物会通 过花冠弯曲 (Sun et al, 2005)、花瓣闭合时雄蕊移动 (Xiong et al, 2013)、异型花 柱向同型花柱转换 (Wang XJ et al, 2021) (Wadgymar et al, 2017;Friedman, 2020;Lundgren & Des Marais, 2020)。研究表明, 高山植物为了应对复杂多变的高 山环境, 往往会将有限的资源在存活和繁殖之间进 行 不 均 等 分 配 , 该 过 程 称 为 分 配 权 衡 (allocation trade-off) (Weiner, 2004;Sun et al, 2014; 张婵等, 2020)。 如果植物将较多的资源分配在提高存活率上, 那么对繁殖方面的投入可能就会相应地减少 (Wenk & Falster, 2015)。以往的研究多集中在探讨高山植 物在有性繁殖和克隆繁殖之间 (Bengtsson & Ceplitis, 2000; 张婵等, 2020)以及交配系统内部(自交与异 交的主次地位)的权衡 Barrett, 2014;Nasrallah, 2017)…”