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Chinese Journal of Plant Ecology >
Gynomonoecy in angiosperms: phylogeny, sex expression and evolutionary significance
Received date: 2013-11-14
Accepted date: 2013-12-19
Online published: 2014-01-15
Gynomonoecy is the mode of sex expression in which female and bisexual flowers occur on the same plants; it is an important step in the evolution of monoecy from hermaphroditism in angiosperms. The sexual system of gynomonoecy is considered to play several important roles, including reducing herbivore damage to pistils, reducing inbreeding depression by favoring out-crossing and pollen-pistil interference, enhancing the flexibility of resource allocation to male and female functions in two flower types, and attracting pollinators. According to the classification of APG III system, gynomonoecy occurs in about 23 families in angiosperms including Lactoridaceae in magnoliids, Araceae and Poaceae in monocots, and Asteraceae, Amaranthaceae, Lamiaceae and other families in eudicots. Gynomonoecy is most common in Asteraceae. Female and bisexual flowers from different gynomonoecious taxa show diversified sex expressions, such as their position in inflorescence, morphs, size and flowering time. These traits are regulated not only by genetic factors, but also by resource availability (e.g., nutrition, light, temperature, and moisture conditions). Because reports on gynomonoecy in China are rare, this paper emphasizes our analysis and summary of the phylogeny of gynomonoecious taxa and their evolution in angiosperm and the relationship between their sex expression and environmental conditions. In addition, five hypotheses on the evolutionary significance of gynomonoecy are introduced and evaluated in this paper. Finally, we discuss prospects for further research in this topical area. Our purpose is to provide a theoretical framework for research on evolutionary patterns and mechanisms of gynomonoecy for angiosperms in China.
Key words： angiosperms; evolutionary significance; gynomonoecy; phylogeny; sex expression; sexual systems
Jannathan MAMUT, TAN Dun-Yan . Gynomonoecy in angiosperms: phylogeny, sex expression and evolutionary significance[J]. Chinese Journal of Plant Ecology, 2014 , 38(1) : 76 -90 . DOI: 10.3724/SP.J.1258.2014.00008
| [1] | Abbott RJ, Schmitt J (1985). Effect of environment on per- centage female ray florets per capitulum and outcrossing potential in a self-compatible composite ( Senecio vulgaris L. var. hibernicus Syme). New Phytologist, 101,219-229. |
| [2] | Andersson H (1999). Female and hermaphrodite flowers on a chimeric gynomonoecious Silene vulgaris plant produce offspring with different genders: a case of heteroplasmic sex determination? Journal of Heredity, 90,563-565. |
| [3] | Ashman TL (2002). The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology, 83,1175-1184. |
| [4] | Bai WN, Zhang DY (2005). Sexual interference in cosexual plants and its evolutionary implications. Acta Phy- toecologica Sinica, 29,672-679. (in Chinese with English abstract) |
| [4] | [ 白伟宁, 张大勇 (2005). 雌雄同体植物的性别干扰及其进化意义. 植物生态学报, 29,672-679.] |
| [5] | Baker HG (1948). Corolla-size in gynodioecious and gynomonoecious species of flowering plants. Proceedings of the Leeds Philosophical and Literary Society (Scientific Section), 5,136-139. |
| [6] | Barlow BA, Forrester J (1984). Pollen tube interactions in Melaleuca. In: Williams EG, Knox RB eds. Pollination ‘84’. University of Melbourne, Parkville. 154-160. |
| [7] | Barrett SCH (1998). The evolution of mating strategies in flowering plants. Trends in Plant Science, 3,335-341. |
| [8] | Barrett SCH (2002a). The evolution of plant sexual diversity. Nature Reviews Genetics, 3,274-284. |
| [9] | Barrett SCH (2002b). Sexual interference of the floral kind. Heredity, 88,154-159. |
| [10] | Bawa KS, Beach JH (1981). Evolution of sexual systems in flowering plants. Annals of the Missouri Botanical Garden, 68,254-274. |
| [11] | Bergh NG, Verboom GA (2011). Anomalous capitulum structure and monoecy may confer flexibility in sex allocation and life history evolution in the Ifloga lineage of paper daisies (Compositae: Gnaphalieae). American Journal of Botany, 98,1113-1127. |
| [12] | Bernardello G, Anderson GJ, Patricio LS, Cleland MA, Stuessy TF, Crawford DJ (1999). Reproductive biology of Lactoris fernandeziana (Lactoridaceae). American Journal of Botany, 86,829-840. |
| [13] | Bertin RI, Connors DB, Kleinman HM (2010). Differential herbivory on disk and ray flowers of gynomonoecious asters and goldenrods (Asteraceae). Biological Journal of the Linnean Society, 101,544-552. |
| [14] | Bertin RI, Gwisc GM (2002). Floral sex ratios and gynomonoecy in Solidago (Asteraceae). Biological Journal of the Linnean Society, 77,413-422. |
| [15] | Bertin RI, Kerwin MA (1998). Floral sex ratios and gynomonoecy in Aster (Asteraceae). American Journal of Botany, 85,235-244. |
| [16] | Bertin RI, Newman CM (1993). Dichogamy in angiosperms. The Botanical Review, 59,112-152. |
| [17] | Bhargava A, Shukla S, Ohri D (2007). Gynomonoecy in Chenopodium quinoa (Chenopodiaceae): variation in inflorescence and floral types in some accessions. Biologia, 62,19-23. |
| [18] | Bullock SH (1985). Breeding systems in the flora of a tropical deciduous forest in Mexico. Biotropica, 17,287-301. |
| [19] | Burtt BL (1977). Aspects of diversification in the capitulum. In: Heywood VH, Harbone JB, Turner BL eds. The Biology and Chemistry of the Compositae. Academic Press, London.41-59. |
| [20] | Cao GX, Kudo G (2008). Size-dependent sex allocation in a monocarpic perennial herb, Cardiocrinum cordatum (Liliaceae). Plant Ecology, 194,99-107. |
| [21] | Carlquist SJ (1974). Island Biology. Columbia University Press, New York. |
| [22] | Casimiro-Soriguer I, Buide ML, Narbona E (2013). The roles of female and hermaphroditic flowers in the gynodio- ecious-gynomonoecious Silene littorea: insights into the phenology of sex expression. Plant Biology, 15,941-947. |
| [23] | Charlesworth D (2006). Evolution of plant breeding systems. Current Biology, 16,R726-R735. |
| [24] | Charlesworth D, Charlesworth B (1978). Population genetics of partial male-sterility and the evolution of monoecy and dioecy. Heredity, 41,137-153. |
| [25] | Champluvier D (1997). Brachystephanus glaberrimus (Acanthaceae), espèce nouvelle gynomono?que de la dorsale Congo-Nil (Congo, Rwanda, Uganda). Bulletin du Jardin botanique national de Belgique / Bulletin van de National Plantentuin van Belgi?, 66,187-200. |
| [26] | Collin CL, Penet L, Shykoff JA (2009). Early inbreeding depression in the sexually polymorphic plant Dianthus sylvestris (Caryophyllaceae): effects of selfing and biparental inbreeding among sex morphs. American Journal of Botany, 96,2279-2287. |
| [27] | Collin CL, Pennings P, Rueffler C, Widmer A, Shykoff JA (2002). Natural enemies and sex: how seed predators and pathogens contribute to sex-differential reproductive suc- cess in a gynodioecious plant. Oecologia, 131,94-102. |
| [28] | Collin CL, Shykoff JA (2003). Outcrossing rates in the gynomonoecious-gynodioecious species Dianthus sylv- estris (Caryophyllaceae). American Journal of Botany, 90,579-585. |
| [29] | Collin CL, Shykoff JA (2010). Flowering phenology and fe- male fitness: impact of a pre-dispersal seed predator on a sexually polymorphic species. Plant Ecology, 206,1-13. |
| [30] | Dai C, Galloway LF (2011). Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species? Functional Ecology, 25,271-278. |
| [31] | Darwin C (1877). The Different Forms of Flowers on Plants of the Same Species. John Murray, London. |
| [32] | Delph LF (1996). Flower size dimorphism in plants with unisexual flowers. In: Lloyd DG, Barrett SCH eds. Floral Biology. Chapman and Hall, New York. 217-237. |
| [33] | Dewald CL, Burson BL, Dewet JMJ, Harlan JR (1987). Morphology, inheritance, and evolutionary significance of sex reversal in Tripsacum dactyloides (Poaceae). American Journal of Botany, 74,1055-1059. |
| [34] | Duarte-Silva E, Vieira MF, Bittencourt NS Jr, Garcia FCP (2010). Polimorfismo floral em Valeriana scandens L. (Valerianaceae). Acta Botanica Brasilica, 24,871-876. |
| [35] | Dufay M, Lahiani E, Brachi B (2010). Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). International Journal of Plant Sciences, 171,53-62. |
| [36] | Field DL, Barrett SCH (2012). Disassortative mating and the maintenance of sexual polymorphism in painted maple. Molecular Ecology, 21,3640-3643. |
| [37] | Folke SH, Delph LF (1997). Environmental and physiological effects on pistillate flower production in Silene noctiflora L. (Caryophyllaceae). International Journal of Plant Sciences, 158,501-509. |
| [38] | Franchi GG, Nepi M, Matthews ML, Pacini E (2007). Anther opening, pollen biology and stigma receptivity in the long blooming species, Parietaria judaica L. (Urticaceae). Flora, 202,118-127. |
| [39] | Ge XY, Zhu BR, Liao WJ (2012). Male biased sex allocation with plant size in gynomonoecious Aster ageratoides. Biodiversity Science, 20,386-390. (in Chinese with English abstract) |
| [39] | [ 戈星月, 朱璧如, 廖万金 (2012). 雌全同株植物三脉紫菀花期偏雄的个体大小依赖的性别分配. 生物多样性, 20,386-390.] |
| [40] | Ghiselin MT (1974). The Economy of Nature and the Evolution of Sex. University of California Press, Berkeley. |
| [41] | Grombone-Guaratini MT, Nascimento AAD, Santos-Gon?alves AP (2011). Flowering and fruiting of Aulonemia aristulata: a gynomonoecious woody bamboo species from Atlantic Forest in Brazil. Revista Brasileira de Botanica, 34,135-140. |
| [42] | Guo YF, Wang YQ, Weber A (2013). Floral ecology of Oreocharis acaulis (Gesneriaceae): an exceptional case of “preanthetic” protogyny combined with approach herkogamy. Flora, 208,58-67. |
| [43] | Hall BK (2003). Evo-Devo: evolutionary developmental mechanisms. International Journal of Developmental Biology, 47,491-495. |
| [44] | Hata N, Murakami K, Yoshida Y, Masuda M (2005). Effect of temperature on expression of gynomonoecy in selfed-seed populations of Spinacia oleracea L. Journal of the Japanese Society for Horticultural Science, 74,228-233. |
| [45] | Hata N, Murakami K, Yoshida Y, Masuda M (2006a). Effect of photoperiod after bolting on the expression of gynomonoecy in Spinacia oleracea L. Journal of the Japanese Society for Horticultural Science, 75,141-147. |
| [46] | Hata N, Murakami K, Yoshida Y, Masuda M, Tanaka A, Shi- kazono N, Hase Y (2006b). Mutagenesis in gyno- monoecious spinach (Spinacia oleracea L.) plants and se- lection of low oxalate variants. Scientific Reports of the Faculty of Agriculture Okayama University, 95,21-28. |
| [47] | Hermanutz LA, Innes DJ (1994). Gender variation in Silene acaulis (Caryophyllaceae). Plant Systematics and Evolution, 191,69-81. |
| [48] | Huang SQ, Guo YH (2000). New advances in pollination biology and the studies in China. Chinese Science Bulletin, 45,1441-1447. |
| [49] | Komai F, Masuda K (2004). Plasticity in sex expression of spinach ( Spinacia oleracea) regenerated from root tissues. Plant Cell, Tissue and Organ Culture, 78,285-287. |
| [50] | Leppik EE (1977). The evolution of capitulum types of the Compositae in the light of insect flower interaction. In: Heywood VH, Harbone JB, Turner BL eds. The Biology and Chemistry of the Compositae. Academic Press, London. 61-89. |
| [51] | Lloyd DG (1972a). Breeding systems in Cotula L. (Compositae, Anthemideae) I. The array of monoclinous and diclinous systems. New Phytologist, 71,1181-1194. |
| [52] | Lloyd DG (1972b). Breeding systems in Cotula L. (Compositae, Anthemideae). II. Monoecious populations. New Phytologist, 71,1195-1202. |
| [53] | Lloyd DG (1979). Parental strategies of angiosperms. New Zealand Journal of Botany, 17,595-606. |
| [54] | Lloyd DG (1980). Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytologist, 86,69-79. |
| [55] | Lloyd DG, Webb CJ (1986). The avoidance of interference between the presentation of pollen and stigma in angiosperms I. Dichogamy. New Zealand Journal of Botany, 24,135-162. |
| [56] | Lowrey TK (1986). A biosystematic revision of Hawaiian Tetramolopium (Compositae: Astereae). Allertonia, 4,203-265. |
| [57] | Lowrey TK, Robinson ER (1988). The interaction of gynomonoecy, dichogamy, and wind-pollination in Gunnera perpensa L. (Gunneraceae) in South Africa. Monographs in Systematic Botany from the Missouri Botanical Garden, 25,237-246. |
| [58] | Lu Y, Huang SQ (2006). Adaptive advantages of gynomonoecious species. Acta Phytotaxonomica Sinica, 44,231-239. (in Chinese with English abstract) |
| [58] | [ 卢洋, 黄双全 (2006). 论雌花两性花同株植物的适应意义. 植物分类学报, 44,231-239.] |
| [59] | Mamut J, Xiong YZ, Tan DY, Huang SQ (2014). Pistillate flowers experience more pollen limitation and less geitonogamy than perfect flowers in a gynomonoecious herb. New Phytologist, 201,670-677. |
| [60] | Mani MS, Saravanan JM (1999). Pollination Ecology and Evolution in Compositae (Asteraceae). Science Publishers, New Hampshire. |
| [61] | Marshall DF, Abbott RJ (1984a). Polymorphism for outcrossing frequency at the ray floret locus in Senecio vulgaris L. II. Confirmation. Heredity, 52,331-336. |
| [62] | Marshall DF, Abbott RJ (1984b). Polymorphism for outcrossing frequency at the ray floret locus in Senecio vulgaris L. III. Causes. Heredity, 53,145-149. |
| [63] | Maurice S (1999). Gynomonoecy in Silene italica (Caryophyllaceae): sexual phenotypes in natural populations. Plant Biology, 1,346-350. |
| [64] | Méndez M, Munzinger J (2010). Planchonella, first record of gynomonoecy for the family Sapotaceae. Plant Systematics and Evolution, 287,65-73. |
| [65] | Molano-Flores B, Danderson CA (2009). Gynomonoecious individuals in Lobelia spicata (Campanulaceae) Populations. Rhodora, 111,398-402. |
| [66] | Muenchow G, Delesalle VA (1992). Patterns of weevil herbivory on male, monoecious and female inflorescences of Sagittaria latifolia. American Midland Naturalist, 127,355-367. |
| [67] | Muenchow GE (1998). Subandrodioecy and male fitness in Sagittaria lancifolia subsp. lancifolia (Alismataceae). American Journal of Botany, 85,513-520. |
| [68] | Müller H (1883). The Fertilization of Flowers. Macmillan, London. |
| [69] | Olesen JM, Forfang AS, Báez M (1998). Stress-induced male sterility and mixed mating in the island plant Cedronella canariensis (Lamiaceae). Plant Systematics and Evolution, 212,159-176. |
| [70] | Onodera Y, Yonaha I, Niikura S, Yamazaki S, Mikami T (2008). Monoecy and gynomonoecy in Spinacia oleracea L.: morphological and genetic analyses. Scientia Horticulturae, 118,266-269. |
| [71] | Palkovic LA (1978). A hybrid of Gunnera from Costa Rica. Systematic Botany, 3,226-235. |
| [72] | Pringle JS (2011). Five new species of South American Gentianella (Gentianaceae). A Journal for Botanical Nomenclature, 21,78-89. |
| [73] | Richards AJ (1997). Plant Breeding Systems. Chapman and Hall, London. |
| [74] | Sun SG, Lu Y, Huang SQ (2006). Floral phenology and sex expression in functionally monoecious Rhoiptelea chiliantha (Rhoipteleaceae). Botanical Journal of the Linnean Society, 152,145-151. |
| [75] | Swenson U, Bremer K (1997). Patterns of floral evolution of four Asteraceae genera (Senecioneae, Blennospermatinae) and the origin of white flowers in New Zealand. Systematic Biology, 46,407-425. |
| [76] | The Angiosperm Phylogeny Group (2009). An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, 161,105-121. |
| [77] | Torices R, Anderberg AA (2009). Phylogenetic analysis of sexual systems in Inuleae (Asteraceae). American Journal of Botany, 96,1011-1019. |
| [78] | Trow AH (1912). On the inheritance of certain characters in the common groundsel—Senecio vulgaris, Linn.—and its segregates. Journal of Genetics, 2,239-276. |
| [79] | Urdampilleta JD, Amat AG, Bidau CJ (2005). Karyotypic studies and morphological analysis of some reproductive features in five species of Conyza (Astereae: Asteraceae) from northeastern Argentina. Boletin de la Sociedad Argentina Botanica, 40,91-99. |
| [80] | Whitkus R, Doan H, Lowrey TK (2000). Genetics of adaptive radiation in Hawaiian species of Tetramolopium (Asteraceae). III. Evolutionary genetics of sex expression. Heredity, 85,37-42. |
| [81] | Willson MF (1983). Plant Reproductive Ecology. John Wiley and Sons, New York. |
| [82] | Wise MJ, Coffey LE, Abrahamson WG (2008). Nutrient stress and gall flies interact to affect floral-sex ratio in gynomonoecious Solidago altissima (Asteraceae). American Journal of Botany, 95,1233-1239. |
| [83] | Yampolsky C, Yampolsky H (1922). Distribution of sex forms in the phanerogamic flora. Bibliotheca Genetica, 3,1-62. |
| [84] | Zhang DY (2004). Plant Life-History Evolution and Reproductive Ecology. Science Press, Beijing. (in Chinese) |
| [84] | [ 张大勇 (2004). 植物生活史进化与繁殖生态学. 科学出版社, 北京.] |
| [85] | Zhang GF, Xie TP, Du GZ (2012). Variation in floral sex allocation, female success, and seed predation within racemiform synflorescence in the gynomonoecious Ligularia virgaurea (Asteraceae). Journal of Plant Research, 125,527-538. |
| [86] | Zhang J, Xu GX, Xue HY, Hu J (2007). Foundation and current progress of plant evolutionary developmental biology. Chinese Bulletin of Botany, 24,1-30. (in Chinese with English abstract) |
| [86] | [ 张剑, 徐桂霞, 薛皓月, 胡瑾 (2007). 植物进化发育生物学的形成与研究进展. 植物学通报, 24,1-30.] |
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