被子植物蜜距的多样性及进化生态学研究

doi:10.17521/cjpe.2022.0445

摘要/Abstract

摘要：

蜜距将花蜜隐藏在距的深处, 多样的蜜距形态和长度吸引各种喙长的传粉动物访花, 促进传粉生态位形成, 这对造就物种多样性起到了重要作用。因此蜜距被认为是促进物种形成的关键创新性状, 是研究被子植物花部结构演化、植物-传粉者协同进化的理想材料。系统地总结蜜距植物及其形态特征和传粉/盗蜜者, 有助于全面了解这一性状在被子植物中的系统发育分布和进化生态学意义。该文对国内外植物分类数据库(检索词“距”或“spur”)和已发表文章(检索词“有距植物属中文名+传粉”或“属拉丁名+ pollinator/nectar robber”)进行系统的梳理和总结, 收集蜜距植物、距长、蜜距形态、传粉者、盗蜜者等信息。整理出具有蜜距的植物分布在被子植物13个目23个科271个属, 共计3 427种。其中蜜距植物种数最多的科为兰科(1 536种)、罂粟科(487种)、毛茛科(351种)、凤仙花科(284种)、堇菜科(197种), 它们占所有蜜距植物种数的83.3%。根据蜜距的发育来源, 蜜距可分为6种类型: 花被片蜜距、花瓣蜜距、萼片蜜距、被丝托蜜距、花萼蜜距和花冠蜜距。花瓣蜜距分布于212个属, 显著高于其他类型。对2 546种植物的蜜距长度分析发现: 凤仙花科的蜜距平均长度最长, 达23.8 mm; 千屈菜科的蜜距最短, 平均仅1.6 mm。形态上, 大部分蜜距具有不同程度的弯曲, 这可能有助于筛选合适的传粉者, 提高访花者的传粉效率; 单花蜜距数量有1-6个, 大部分为1个, 多个蜜距可能增加传粉者的访花时间; 部分兰科和堇菜科植物蜜距内部具有可能分泌花蜜的附属物。蜜距植物的传粉者主要为膜翅目、鳞翅目、部分长喙双翅目昆虫及鸟类; 盗蜜者主要为膜翅目昆虫。蜜距的长度和传粉者的喙长普遍存在地理镶嵌的协同进化关系, 进化生态学家提出了“达尔文机械模型”的假说来解释这种现象; 而当传粉者喙长不变, 距长随着传粉者种类改变时则用“传粉者转变模型”来解释蜜距的伸长。未来在蜜距的进化生态学研究中, 不仅要关注蜜距植物的距长和传粉者喙长的形态学特征及传粉生态学研究, 还应借助发育解剖学和基因组学, 以及新的技术手段, 从细胞的分裂、伸长, 功能基因, 非生物因子等各个方面, 探索蜜距演化的驱动因素。

关键词: 蜜距, 距长, 关键创新性状, 花部结构, 盗蜜

Abstract:

For many plants, nectar is hidden in the depth of nectar spurs. The diverse morphology and length of nectar spurs can attract pollinators with various proboscis lengths and promote the differentiation of pollination niche, which plays an important role in the formation of species diversity. Therefore, nectar spur is considered as a key innovation trait in promoting speciation and an ideal trait for studying floral evolution and plant-pollinator coevolution in angiosperm. This review systematically summarizes the worldwide plant taxonomic databases and published articles, classifies the nectar spur plants, and reviews the diversity and evolutionary mechanisms of nectar spur plants. We investigated 3 427 nectar spur species belonging to 13 orders, 23 families and 271 genera of angiosperm. Among them, Orchidaceae has the largest number of species, with 1 536 species, following by Papaveraceae with 487 species, Ranunculaceae with 351 species, Balsaminaceae with 284 species and Violaceae with 197 species, accounting for 83.3% of all the species. According to the sources of the development of nectar spurs, the nectar spurs can be divided into six types: petal spur, corolla spur, sepal spur, calyx spur, tepal spur and hypanthium spur. The petal spurs are the predominant type, detected in 212 genera. The average length of nectar spurs in Balsaminaceae is the longest (23.8 mm) among the 2 546 species whose nectar spurs have been measured. The shortest nectar spurs are reported in Lycelandaceae, which are only 1.6 mm on average. Most nectar spurs have different degrees of curvature, likely helping to improve the pollination efficiency. The number of nectar spur(s) in a flower ranges from 1 to 6, and most species have only one nectar spur in a flower. Multiple nectar spurs may increase the visiting time of pollinators. Some plants in Orchidaceae and Violaceae have appendages inside the nectar spurs, which may have the function of nectar secretion. The pollinators of plants with nectar spur mainly comprise insects from Hymenoptera, Lepidoptera, and some long-proboscis species from Diptera and birds. Nectar robbers are mainly bees and birds. There is a general association of geographic mosaic theory of coevolution between the length of nectar spur and the length of pollinator proboscis. Evolutionary ecologists have proposed the hypothesis of “Darwin’s Mechanistic Model” and “The Pollinator Shift Model” to explain this phenomenon. In future studies of the mechanisms of nectar spur evolution, we should not only focus on the morphological characteristics of spur length and proboscis length and the pollination ecology, but also explore the driving forces of nectar spurs evolution from cell division/elongation, functional genes, abiotic factors, with the help of novel technological approaches including developmental anatomy and genomics.

Key words: nectar spur, spur length, key evolutionary innovation, floral structure, nectar robbing

杨明威, 金晓芳. 被子植物蜜距的多样性及进化生态学研究. 植物生态学报, 2023, 47(9): 1193-1210. DOI: 10.17521/cjpe.2022.0445

YANG Ming-Wei, JIN Xiao-Fang. Diversity and evolutionary ecology of nectar spurs in angiosperms. Chinese Journal of Plant Ecology, 2023, 47(9): 1193-1210. DOI: 10.17521/cjpe.2022.0445

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0445

https://www.plant-ecology.com/CN/Y2023/V47/I9/1193

图/表 6

图1 被子植物蜜距的多样性。A, 二叶舌唇兰(兰科)。B, 木鱼坪淫羊藿(小檗科)。C, 中甸乌头(毛茛科)。D, 华北耧斗菜(毛茛科)。E, 早开堇菜(堇菜科)。F, 囊距紫堇(罂粟科)。G, 大花花锚(龙胆科)。H, 摩洛哥柳穿鱼(车前科)。I, 黄花狸藻(狸藻科)。J, 凤仙花属(凤仙花科)。K, 油点草(百合科)。L, 旱金莲(旱金莲科)。其中A-F为花瓣蜜距, G-I为花冠蜜距, J为萼片蜜距, K为花被片蜜距, L为被丝托蜜距。白色箭头所指为各种形态的蜜距。拍摄者: 金晓芳。

Fig. 1 Diversity of nectar spurs in angiosperms. A, Platanthera chlorantha (Orchidaceae). B, Epimedium franchetii (Berberidaceae). C, Aconitum piepunense (Ranunculaceae). D, Aquilegia yabeana (Ranunculaceae). E, Viola prionantha (Violaceae). F, Corydalis benecincta (Papaveraceae). G, Halenia elliptica var. grandiflora (Gentianaceae). H, Linaria maroccana (Plantaginaceae). I, Utricularia aurea (Lentibulariaceae). J, Impatiens sp. (Balsaminaceae). K, Tricyrtis macropoda (Liliaceae). L, Tropaeolum majus (Tropaeolaceae). A-F are petal spurs, G-I are corolla spurs, J is sepal spur, K is tepal spur, and L is hypanthium spur. The white arrows indicate the various forms of the nectar spurs. Photoed by JIN Xiao-Fang.

表1 被子植物蜜距的发育来源及其系统分布

Table 1 Origin and phylogenetic distribution of nectar spurs in angiosperms

图2 花瓣卷缩形成的蜜距(翠雀属、乌头属)和被丝托蜜距的结构解剖。A, 中甸乌头的花瓣蜜距。B, 中甸翠雀花的花瓣蜜距(被包裹在萼距里面)。C, 旱金莲的被丝托蜜距。NS, 蜜距; P, 花瓣; S, 萼片。拍摄者: 金晓芳。

Fig. 2 Nectar spur formed by petal rolling (Aconitum, Delphinium) and hypanthium spur. A, Petal spur of A. piepunense. B, Petal spur of D. yuanum (encased in calyx spur). C, Hypanthium spur of Tropaeolum majus. NS, nectar spur; P, petal; S, sepal. Photoed by JIN Xiao-Fang.

图3 被子植物蜜距在目一级的系统发育分布。系统树根据Angiosperm phylogeny poster (APP)—Flowering plant systematics, 2019绘制(Cole et al., 2019)。线描图红色部分为蜜距所在位置。植物科和蜜距类型所附括号内为距长变异系数和样本量。两列箱型图分别为17个科和6种蜜距类型的蜜距长度log值(平均值±标准差)。

Fig. 3 Distribution of nectar spur types across angiosperm orders. The phylogeny of angiosperm orders is drawn according to the Angiosperm phylogeny poster (APP)—Flowering plant systematics, 2019 (Cole et al., 2019). The red parts of the line diagrams show the location of the nectar spurs. Coefficient of variation of spur length and sample size are enclosed in parentheses for plant families and nectar spur types. The log values (mean ± SD) of spur length for 17 families and 6 types of nectar spur are shown in the two box plots.

表2 距长变异系数与距长其他特征的相关分析统计结果

Table 2 Statistical results of correlation analysis between the coefficient of variation of nectar spur length with other characteristics

	标准差 Standard deviation		平均值 Average value		数据量 Amount of data		传粉者属数 Genus number of pollinators
	r	p	r	p	r	p	r	p
蜜距类型 Type of nectar spur	0.781	0.067	0.563	0.245	0.542	0.266	0.413	0.416
科 Family	0.889	<0.001	0.502	0.034	0.716	<0.001	0.752	<0.001
属 Genus	0.699	<0.001	0.371	0.107	0.099	0.679	-0.079	0.808

图4 蜜距植物的主要访花者和盗蜜者。A, 南熊蜂访中甸翠雀花。B, 独居蜂访柔毛淫羊藿。C, 条蜂访刻叶紫堇。D, 熊蜂访椭圆叶花锚。E, 熊蜂访顶喙凤仙花。F, 条蜂访摩洛哥柳穿鱼。G, 条蜂盗蜜地锦苗。H, 黄胸木蜂盗蜜凤仙花。拍摄者: 金晓芳。

Fig. 4 Pollinators and nectar robbers of some plants with nectar spurs. A, Bombus secures visiting Delphinium yuanum. B, Solitary bee visiting Epimedium pubescens. C, Anthophoridae bee visiting Corydalis incisa. D, Bombus sp. visiting Halenia elliptica. E, Bombus sp. visiting Impatiens compta. F, Anthophoridae bee visiting Linaria maroccana. G, Anthophoridae bee robbing nectar of Corydalis sheareri. H, Xylocopa appendiculata robbing nectar of Impatiens balsamina. Photoed by JIN Xiao-Fang.

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