Chin J Plan Ecolo ›› 2018, Vol. 42 ›› Issue (8): 806-817.doi: 10.17521/cjpe.2018.0053

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Diversity and evolution of samara in angiosperm

TAN Ke,DONG Shu-Peng,LU Tao,ZHANG Ya-Jing,XU Shi-Tao,REN Ming-Xun()   

  1. Center for Terrestrial Biodiversity of the South China Sea, Institute of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China
  • Received:2018-03-05 Online:2018-12-07 Published:2018-08-20
  • Contact: Ming-Xun REN E-mail:jshe@pku.edu.cn
  • Supported by:
    Supported by the National Natural Science Foundation of China(31670230);Supported by the National Natural Science Foundation of China(31660229);the Innovative Team Program of Hainan Natural Science Foundation(2018CXTD334);the Postgraduate Innovative Grant of Hainan Province(Hyb2016-06)

Abstract:

Samara (winged fruit) can be dispersed easily by wind and may be a crucial factor for angiosperm spread and diversification. In a narrow sense, a samara is an indehiscent dry fruit with wing(s) developed from fruit pericarp, while in a broad sense samaras also include all winged fruits with wings developed from both pericarp and perianth or bracts. According to the wing shape and growth patterns of samaras, we divided samaras into six types, i.e. single-winged, lanceolate-winged, rib-winged, sepal-winged, bract-winged, and perigynous samaras. Perigynous samaras can be further classified into two forms, i.e. round-winged and butterfly-winged samaras. Accordingly, the aerodynamic behavior of samaras can be classified into five types, autogyro, rolling autogyro, undulator, helicopter, and tumbler. The rib-winged and round-winged samaras can be found in Laurales, a basal angiosperm, and may represent the primitive type of early samaras. In the derived clades, samaras evolved enlarged but unequal wings and decreased wing loading (the ratio of fruit weight to wing size), which is likely an adaptation to gentle wind and secondary dispersal through water or ground wind. The wings of some samaras (such as sepal-winged and bract-winged samaras) may have multiple functions including wind dispersal, physical defense for the seeds, and adjust seed germination strategy. The pantropical family Malpighiaceae is extraordinarily rich in samara types, which is likely related to its multiple inter-continent dispersal in history, which is known as “Malpighiaceae Route”. Therefore, Malpighiaceae can be used as a model system for the studies on samara adaptation and evolution. We identified the following issues that deserve further examination in future studies using both ecological and evo-devo methods: 1) the adaption of different types of samaras in dispersal processes, 2) the molecular and developmental mechanism of sepal- and bract-wings, and 3) the evolution of samara types and their effects on angiosperm diversification.

Key words: samara, long-distance dispersal, Malpighiaceae Route, adaptive evolution

Fig. 1

Six types of samaras of angiosperms. (Green, 1980; Augspurger, 1986; Peck & Lersten, 1991)。"

Table 1

The six types of angiosperm samaras and their systematic distribution"

翅果类型 Samara type 主要分布类群 Systematic distribution
1 单侧翅果 Single-winged samara (SWS)
1.1 单翅果
Mono-SWS
金虎尾科(异翅藤属, Acridocarpus, Banisteriopsis, Barnebya, Bronwenia, Cordobia, Cottsia, Dinemagonum, Diplopterys, Ectopopterys, Janusia, Peixotoa, Sphedamnocarpus, Stigmaphyllon), 木犀科陉属, 远志科蝉翼藤属, 鼠李科翼核果属, 榆科刺榆属, 梧桐科银叶树属
Malpighiaceae (Heteropterys, Acridocarpus, Banisteriopsis, Barnebya, Bronwenia, Cordobia, Cottsia, Dinemagonum, Diplopterys, Ectopopterys, Janusia, Peixotoa, Sphedamnocarpus, Stigmaphyllon), Fraxinus (Oleaceae), Securidaca (Polygalaceae), Ventilago (Rhamnaceae), Hemiptelea (Ulmaceae), Heritiera (Sterculiaceae)
1.2 双聚单翅果 Di-SWS 槭树科槭树属, 木犀科陉属
Acer (Aceraceae), Fraxinus (Oleaceae)
1.3 三聚单翅果 Tri-SWS 金虎尾科翅实藤属, 异翅藤属
Malpighiaceae (Ryssopterys, Heteropterys)
2 周位翅果 Perigynous samara
2.1 圆翅果
Round-winged samara
金虎尾科(盾翅藤属, Alicia, Amorimia, Calcicola, Caucanthus, Christianella, Diaspis, Excentradenia, Flabellaria, Madagasikaria, Malpighiodes, Mascagnia, Mezia), 胡桃科(青钱柳属, 化香树属), 豆科(紫檀属, 黄檀属), 十字花科(菘蓝属, 屈曲花属, 菥属), 桦木科(桤木属, 桦木属), 榆科(榆属, 青檀属), 蓼科山蓼属, 木樨科雪柳属, 槭树科金钱槭属, 苦木科臭椿属, 杜仲科杜仲属, 芸香科榆橘属, 蓝果树科喜树属, 莲叶桐科青藤属, 鼠李科马甲子属, 马尾树科马尾树属
Malpighiaceae (Aspidopterys, Alicia, Amorimia, Calcicola, Caucanthus, Christianella, Diaspis, Excentradenia, Flabellaria, Madagasikaria, Malpighiodes, Mascagnia, Mezia), Juglandaceae (Cyclocarya, Platycarya), Fabaceae (Pterocarpus, Dalbergia), Cruciferae (Isatis, Iberis, Thlaspi), Betulaceae (Alnus, Betula), Ulmaceae (Ulmus, Pteroceltis), Oxyria (Polygonaceae), Fontanesia (Oleaceae), Dipteronia (Aceraceae), Ailanthus (Simaroubaceae), Eucommia (Eucommiaceae), Ptelea (Rutaceae), Camptotheca (Nyssaceae), Illigera (Hernandiaceae), Paliurus (Rhamnaceae), Rhoiptelea (Rhoipteleaceae)
2.2 蝶翅果
Butterfly-winged samara
金虎尾科(Adelphia, Aenigmatanthera, Hiraea, Amorimia, Callaeum, Carolus, Christianella, Dinemandra等), 菊科(金鸡菊属, 偶雏菊属, 蟛蜞菊属), 木犀科(雪柳属, 六道木叶属), 使君子科(诃子属, 榆绿木属, 假榆橘属)
Malpighiaceae (Adelphia, Christianella, Aenigmatanthera, Hiraea, Amorimia, Callaeum, Carolus, Dinemandra, etc.), Asterceae (Coreopsis, Boltonia, Sphagneticola), Oleaceae (Fontanesia, Abeliophyllum), Combretaeeae (Terminalia, Anogeissus, Pteleopsis)
3 棱翅果
Rib-winged samara
金虎尾科(Aspicarpa, Calcicola, Digoniopterys), 蓼科(翅果蓼属, 红药子属, 大黄属, 沙拐枣属, 等), 卫矛科(雷公藤属, 卫矛属, 等), 使君子科(风车子属, 诃子属), 无患子科(车桑子属, 黄梨木属), 椴树科(滇桐属, 蚬木属, 柄翅果属, 一担柴属), 鼠李科咀签属, 莲叶桐科青藤属, 茶茱萸科心翼果属, 薯蓣科薯蓣属, 藜科四翅滨藜, 胡颓子科翅果油树
Malpighiaceae (Aspicarpa, Calcicola, Digoniopterys), Polygonaceae (Parapteropyrum, Pteroxygonum, Rheum, Calligonum etc.), Celastraceae (Tripterygium, Euonymus etc.), Sapindaceae (Dodonaea, Boniodendron), Tiliaceae (Craigia, Excentrodendron, Burretiodendron, Colona), Gouania (Rhamnaceae), Illigera (Hernandiaceae), Cardiopteris (Icacinaceae), Dioscorea (Dioscoreaceae), Atriplex canescens (Chenopodiaceae), Elaeagnus mollis (Elaeagnaceae)
4 披针翅果
Lanceolate-winged samara
金虎尾科(风筝果属, 三星果属, Lophopterys, Dicella, Microsteira, Niedenzuella, Rhynchophora, Tetrapterys), 椴树科六翅木属, 卫矛科斜翼属, 十字花科沙芥属, 使君子科萼翅藤属
Malpighiaceae (Hiptage, Tristellateia, Lophopterys, Dicella, Microsteira, Niedenzuella, Rhynchophora, Tetrapterys), Berrya (Tiliaceae), Plagiopteron (Celastraceae), Pugionium (Crucificeae), Getonia (Combretaeeae)
5 翼状萼翅果
Sepal-winged samara
龙脑香科, 钩枝藤科钩枝藤属, 旋花科(飞蛾藤属, 三翅藤属, 白花叶属, 地旋花属)
Dipterocarpaceae, Ancistrocladus (Ancistrocladaceae), Convolvulaceae (Dinetus, Tridynamia, Poranopsis, Xenostegia)
6 叶状苞翅果
Bract-winged samara
桦木科(鹅耳枥属, 铁木属, 桦木属, 桤木属, 榛属), 胡桃科(黄杞属, 枫杨属), 败酱科败酱属, 旋花科盾苞藤属, 马鞭草科楔翅藤属, 檀香科米面蓊属
Betulaceae (Carpinus, Ostrya, Betula, Alnus, Corylus), Juglandaceae (Engelhardia, Pterocarya), Patrinia (Valerianaceae), Neuropeltis (Convolvulaceae), Sphenodesme (Verbenaceae), Buckleya (Santalaceae)

Fig. 2

The systematic distribution of samara types across angiosperm orders. The phylogeny of angiosperm orders was drawn according to the Angiosperm Phylogeny Group (2016)."

Fig. 3

Samara diversity and evolution in Malpighiaceae. Note there has evolutionary transition of samara types for each long-distance dispersal between continents. The phylogeny is redrawn from Davis et al. (2014)."

Fig. 4

Descent velocity and its relationship with wing loading (fruit mass / wing size) of samaras and pollen grains. Revised from Augspurger (1986)."

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