“金虎尾路线”植物的花进化与传粉转变

doi:10.17520/biods.2015195

摘要/Abstract

摘要：

以金虎尾科植物地理分布格局及迁移历史总结出来的“金虎尾路线”, 是解释热带植物洲际间断分布与长距离扩散格局的重要模式。金虎尾路线阐明了金虎尾科植物历史时期7次独立的从起源中心(南美洲)向旧世界(非洲和亚洲)的洲际长距离扩散事件。本文总结了金虎尾路线植物起源地与扩散地主要类群的花部特征与传粉系统, 以探讨这些类群及类似植物长距离扩散后的花进化与传粉转变等适应规律。金虎尾科的南美洲类群都有分泌油脂的萼片腺体, 花的形态结构非常保守, 是与美洲当地特有的条蜂科集油蜂长期协同进化的结果。金虎尾科的非洲类群花保守性消失, 花白色、辐射对称且无萼片腺体, 繁育系统为雄花-两性花异株(功能性的雌雄异株), 传粉者是采集花粉的蜜蜂科昆虫。亚洲的一些属发生了类似非洲类群的泛化适应转变, 但风筝果属(Hiptage)出现了镜像花、异型雄蕊和极度反折的花瓣, 且传粉者是亚洲特有的大蜜蜂(Apis dorsata), 显示出了非常特化的适应性转变。风筝果属所在支系的现存类群涵盖了南美洲、中美洲、非洲和亚洲等地的地方特有属, 体现了金虎尾路线整个迁移历史过程, 是认识金虎尾路线及其进化适应规律的关键类群, 值得在今后的研究中加以重视。

关键词: 适应进化, 繁育系统, 长距离扩散, 间断分布, Malpighiaceae

Abstract

The “Malpighiaceae route” is proposed based on the distribution pattern of the family Malpighiaceae to explain plant inter-continent disjunctions and long-distance dispersal during historical periods. The route involves seven inter-continent dispersals from New World (America) to Old World (Africa and Asia) in the Eocene (~ 65 Ma). Malpighiaceae has about 1,300 species, most of which are endemic to the New World and are characterized by “floral conservatism”. Floral conservatism in this family refers to its stereotyped yellow or pink flowers with paired oil-glands on each sepal, a result from co-evolution with specialized oil-collecting Anthophoridae bees. These bees, however, are absent from the Old World. In the African Malpighiaceae, floral conservatism disappeared as a result of adaptations to local pollen-collecting bees. Their flowers became white and radially symmetric, without sepal gland. Furthermore, the floral sex changed to be morphological androdioecy but functional dioecy. These results indicated that African Malpighiaceae had shifted from floral conservatism to generalized floral syndromes. In Asian Malpighiaceae, some studies reported in Aspidopterys and Ryssopterys generalized evolutionary adaptations in floral traits and pollination systems similar to African taxa. But a recent study found mirror-image flowers, a highly-specialized pollination system, in the Asia-endemic genus Hiptage. Mirror-image flowers in Hiptage show a sexual polymorphism in which the style deflects either to the left or the right side of the floral axis, which is a highly specialized mechanism promoting cross-pollination between left- and right-styled flowers via pollinators touching two sexual organs respectively with their left and right side of abdomens. Hiptage is also notable for its heteromorphic stamens, bilaterally-symmetric corolla, and extremely-reflected petals. Its main pollinators are the pollen-collecting honeybees such as Apis dorsata. These results indicate that the Asian Malpighiaceae could shift from floral conservatism to specialized pollination systems adapted to pollen-gathering honeybees. Hiptage is also distinctive for its position in a clade with complete migration history of Malpighiaceae route, having endemic genera respectively in South and Central America, Africa, and Asia. Further experimental studies on this genus and other Asia-endemic genera are needed to fully understand the Malpighiaceae route and its associated evolutionary adaptations, which will be helpful for studies on plant long-distance dispersal and inter-continent disjunctions.

Key words: adaptive evolution, breeding systems, long-distance dispersal, disjunction, Malpighiaceae

钱贞娜, 任明迅 (2016) “金虎尾路线”植物的花进化与传粉转变. 生物多样性, 24, 95-101. DOI: 10.17520/biods.2015195.

Zhenna Qian, Mingxun Ren (2016) Floral evolution and pollination shifts of the “Malpighiaceae route” taxa, a classical model for biogeographical study. Biodiversity Science, 24, 95-101. DOI: 10.17520/biods.2015195.

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https://www.biodiversity-science.net/CN/Y2016/V24/I1/95

图/表 4

图1 金虎尾路线示意图。金虎尾科植物起源于大约75 Ma的南美洲北部, 之后逐渐迁移至北美洲, 再通过北大西洋陆桥扩散到劳亚古陆及后来的非洲与亚洲等地(背景地图为约65 Ma的始新世)。扩散路线旁的数字为大约的发生时间(根据Davis et al, 2010, 2014)。

Fig. 1 The sketch map of “Malpighiaceae route”. The family is proposed to be originated at about 75 Ma at the north of South America and its current distributions are proposed to have resulted by migration from South America to the Old World via land bridges in North Atlantic Ocean during Eocene (~ 65 Ma). The time near the dispersal route is adapted from Davis et al (2010, 2014).

图2 “金虎尾路线”包括了7次历史时期的从美洲(南美洲、中美洲)到旧世界(非洲、亚洲)的长距离扩散事件。金虎尾科另有2次最近发生的美洲-非洲西海岸的直接横渡大西洋的迁移(★)。系统树及迁移历史时间根据Davis等(2014)。

Fig. 2 Malpighiaceae migrate independently into Old World (Africa and Asia) from South and Central America a total of seven times in the ancient time, with two very recent arrives to the west coast of Africa directly across the Atlantic Ocean (★). Phylogeny tree and the dispersal time are obtained from Davis et al (2014).

表1 金虎尾科植物在不同大洲的主要花部特征、繁育系统及传粉者

Table 1 Breeding system, floral syndromes and pollinators of Malpighiaceae in different continents

	繁育系统 Breeding system	花对称性 Floral symmetry	花萼腺体 Calyx glands	传粉者 Pollinators	参考文献 References
南美洲 South America	两性花 Hermaphrodite	两侧对称 Bilateral symmetry	10个油脂腺体 (每个萼片2个) 10 oil glands, paired on each sepal	美洲特有的条蜂科集油蜂 America-endemic oil-collecting bees, including Centridini, Tetrapediini, and Tapinotaspidini	Anderson, 1979; Davis & Anderson, 2010; Davis et al, 2014
中美洲、北美洲 Central and North America	两性花(闭花受精) Hermaphrodite (cleistogamy)	辐射对称 Radial symmetry	无 None	花内自交, 不需传粉者 Autogamy (pollinator not needed)	Anderson, 1980
非洲 Africa	雄花两性花异株(功能性雌雄异株) Androdioecy (functional dioecy)	辐射对称 Radial symmetry	无 None	收集花粉的蜜蜂科昆虫 Pollen-gathering bees	Davis, 2002; Davis et al, 2014
亚洲 Asia	两性花(镜像花) Hermaphrodite (mirror- image flowers)	两侧对称 Bilateral symmetry	无或1 (如有, 分泌糖) None or single (if present, secretes nectar)	收集花粉的大蜜蜂(Apis dorsata) Asian giant bees (Apis dorsata) collecting pollen	Ren et al, 2013; Ren, 2015

图3 亚洲特有的风筝果属(Hiptage)的分化与迁移历史是整个金虎尾路线扩散路径最完整、最具代表性的支系, 现存类群在南美洲、中美洲、非洲以及亚洲都有各自特有属(属名后为该属物种数)。系统树改自Davis和Anderson (2010)。

Fig. 3 The Asia-endemic Hiptage is in the clade with complete migration history of Malpighiaceae route, having endemic genera respectively in America, Africa, and Asia. The number in the brackets is the species diversity of the genus. Phylogeny relationships are determined according to Davis & Anderson (2010).

参考文献 27

1	Anderson WR (1979) Floral conservatism in neotropical Malpighiaceae. Biotropica, 11, 219-223.
2	Anderson WR (1980) Cryptic self-fertilization in the Malpighiaceae. Science, 207, 892-893.
3	Anderson WR (1981) Malpighiaceae in the botany of the Guayana Highland. Part XI. Memoirs of the New York Botanical Garden, 32, 45-48.
4	Anderson WR (1990) The origin of the Malpighiaceae: the evidence from morphology. Memoirs of the New York Botanical Garden, 64, 210-224.
5	Anderson WR, Anderson C, Davis CC (2006) Malpighiaceae.[accessed <date-in-citation content-type="access-date">2015-06-19</date-in-citation>]
6	Cappellari SC, Haleem MA, Marsaioli AJ, Tidon R, Simpson BB (2011) Pterandra pyroidea: a case of pollination shift within Neotropical Malpighiaceae. Annals of Botany, 107, 1323-1334.
7	Chanderbali AS, van der Werff H, Renner SS (2001) Phylogeny and historical biogeography of Lauraeeae: evidence from the chloroplast and nuclear genomes. Annals of Missouri Botanical Garden, 88, 104-134.
8	Chen SK, Funton AM (2008) Malpighiaceae. In: Flora of China, Volume 11 (Eds Wu ZY, Raven PH, Hong DY), pp. 135-138. Science Press, Beijing & Missouri Botanical Garden Press, St. Luis.
9	Davis CC (2002) Madagasikaria (Malpighiaceae): a new genus from Madagascar with implications for floral evolution in Malpighiaceae. American Journal of Botany, 89, 699-706.
10	Davis CC, Bell CD, Mathews S, Donoghue MJ (2002) Laurasian migration explains Gondwanan disjunctions: evidence from Malpighiaceae. Proceedings of the National Academy of Sciences, USA, 99, 6833-6837.
11	Davis CC, Anderson WR (2010) A complete generic phylogeny of Malpighiaceae inferred from nucleotide sequence data and morphology. American Journal of Botany, 97, 2031-2048.
12	Davis CC, Schaefer H, Xi ZX, Baum DA, Donoghue MJ, Harmon LJ (2014) Long-term morphological stasis maintained by a plant-pollinator mutualism. Proceedings of the National Academy of Sciences, USA, 111, 5914-5919.
13	Fritseh PW (2001) Phylogeny and biogeography of the flowering plant genus Styrax (Styraeaceae) based on chloroplast DNA restriction sites and DNA sequences of the internal transeribed spacer region. Molecular Phylogenetics and Evolution, 19, 387-408.
14	Gates B (1982) Banisteriopsis, Diplopterys (Malpighiaceae). Flora Neotropica, 30, 1-237.
15	Jesson LK, Barrett SCH (2002) Solving the puzzle of mirror-image flowers. Nature, 417, 707.
16	Jesson LK, Barrett SCH (2003) The comparative biology of mirror-image flowers. International Journal of Plant Sciences, 164, 237-249.
17	Lin Y, Tan DY (2007) Enantiostyly in angiosperms and its evolutionary significance. Acta phytotaxonomica Sinica, 45, 901-916. (in Chinese with English abstract)
	[林玉, 谭敦炎(2007) 被子植物镜像花柱及其进化意义. 植物分类学报, 45, 901-916.]
18	Ren MX (2015) The upper reaches of the largest river in Southern China as an ‘evolutionary front’ of tropical plants: evidences from Asia-endemic genus Hiptage (Malpighiaceae). Collectanea Botanica, 34, e002.
19	Ren MX, Zhang DY (2004) Herkogamy. In: Plant Life-History Evolution and Reproductive Ecology (ed. Zhang DY), pp. 303-320. Science Press, Beijing. (in Chinese)
	[任明迅, 张大勇 (2004) 雌雄异位. 见: 植物生活史进化与繁殖生态学 (张大勇主编). 科学出版社, 北京.]
20	Ren MX, Zhong YF, Song XQ (2013) Mirror-image flowers without buzz pollination in the Asia-endemic Hiptage benghalensis (Malpighiaceae). Botanical Journal of the Linnean Society, 173, 764-774.
21	Renner SS, Clausing G, Meyer K (2001) Historical biogeography of Melastomataceae: the roles of tertiary migration and long-distance dispersal. American Journal of Botany, 88, 1290-1300.
22	Renner SS, Schaefer H (2010) The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philosophical Transactions of the Royal Society of London, Series B, 365, 423-435.
23	Steiner KE (1985) Functional dioecism in the Malpighiaceae: The breeding system of Spachea membranacea Cuatr. American Journal of Botany, 72, 1537-1543.
24	Vogel S (1990) History of the Malpighiaceae in the light of pollination ecology. Memoirs of the New York Botanical Garden, 55, 130-142.
25	Week A, Daly AW, Simpson BB (2005) The phylogenetic history and biogeography of the frankincense and myrrh family (Burseraeeae) based on nuclear and chloroplast sequence data. Molecular Phylogenetics and Evolution, 35, 85-101.
26	Zhang WH, Kramer EM, Davis CC (2010) Floral symmetry genes and the origin and maintenance of zygomorphy in a plant-pollinator mutualism. Proceedings of the National Academy of Sciences, USA, 107, 6388-6393.
27	Zhou ZK, Yang XF, Yang QS (2006) Land bridge and long-distance dispersal—old ideas, new evidence. Chinese Science Bulletin, 51, 897-886. (in Chinese)
	[周浙昆, 杨雪飞, 杨青松 (2006) 陆桥说和长距离扩散——老观点, 新证据. 科学通报, 51, 879-886.]

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