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Heterodichogamy.Pdf

Heterodichogamy.Pdf

Research Update TRENDS in Ecology & Evolution Vol.16 No.11 November 2001 595

How common is heterodichogamy? Susanne S. Renner

The sexual systems of usually Heterodichogamy differs from normal (). These figures probably depend on the exact spatial distribution of dichogamy, the temporal separation of underestimate the frequency of the gamete-producing structures. Less well male and female function in , in heterodichogamy. First, the phenomenon known is how the exact timing of male and that it involves two genetic morphs that is discovered only if behavior is female function might influence occur at a 1:1 ratio. The phenomenon was studied in several individuals and in mating. New papers by Li et al. on a group discovered in walnuts and hazelnuts5,6 natural populations. Differential of tropical gingers describe differential (the latter ending a series of Letters to movements and maturation of petals, maturing of male and female structures, the Editor about hazel flowering that styles, stigmas and become such that half the individuals of a began in Nature in 1870), but has gone invisible in dried herbarium material, population are in the female stage when almost unnoticed7. Indeed, its recent and planted populations deriving from the other half is in the male stage. This discovery in Alpinia was greeted as a vegetatively propagated material no new case of heterodichogamy is unique new mechanism, differing ‘from other longer reflect natural morph ratios. The in involving reciprocal movement of the passive outbreeding devices, such as discovery of heterodichogamy thus styles in the two temporal morphs. dichogamy…and heterostyly in that it depends on field observations. Second, combines some features of all of these many dichogamous exhibit Most of the 250 000 species of flowering mechanisms with the unique movement so-called synchronous dichogamy, the plants keep inbreeding to a minimum of floral parts’1. situation that flowers of an individual by genetic self incompatibility or all mature in synchrony, with little or morphological outcrossing mechanisms. no overlap between carpellate and Of the morphological outcrossing staminate stages. Completely mechanisms, dioecy and heterostyly have synchronous flower development received much attention, whereas others, has been described from species of such as androdioecy, have never been Acer (Sapindaceae), Bomarea analyzed comprehensively. The recent (Amaryllidaceae), Ficus (Moraceae), discovery by Li et al.1–3 of an intricate Pentagonia (Rubiaceae), , outcrossing mechanism in Alpinia, a Apiaceae, Araliaceae and many other of Zingiberaceae, now highlights genera and families8–10. Such what is possibly the least-understood developmental synchrony among the angiosperm sexual system. sexual stages of flowers requires that Populations of Alpinia comprise two plants are out of phase with each other genetic morphs. One sheds in the for successful to occur, and morning and has stigmas exposed to this is indeed the case11. The factors pollinators in the afternoon, the other controlling within-plant synchrony and sheds pollen in the afternoon and has between-plant asynchrony are poorly stigmas exposed to pollinators in the understood, but it is clear that time- morning (Fig. 1). The stigmas are brought lagged individuals in ‘normal’ into the ‘right’ position by differential synchronously dichogamous species do growth of the style. Styles of flowers that not have genetically determined morphs. shed pollen in the morning are initially Genetically determined temporal curved upward so that their stigmas do Fig. 1. Flower of Alpinia bracteata showing an upward- dimorphism comes in two forms. In the not contact the nectar-foraging bees that curved style. At around noon, this style will begin to simplest case, flowers in the two morphs pollinate Alpinia. At around noon, they curve downwards, bringing the into a position open 6, 12, or 24 h apart. For example, one where it will contact incoming bees and receive pollen. begin to grow and curve downwards, Photograph reproduced, with permission, from morph might open flowers with receptive bringing the stigmas into a position where Qing-Jun Li. stigmas in the morning and shed pollen they will contact incoming bees and in the afternoon or the next morning receive pollen. This female stage lasts A review of the literature shows that (depending on species; see Table 1). The from about 4:40 pm until dark, when the heterodichogamy is phylogenetically complementary morph opens flowers in flowers wilt. The reciprocal morph has widespread, occurring in nine orders, the afternoon and sheds pollen the next styles first curved downwards, then 11 families, and 17 genera of flowering morning or afternoon. This is the case in growing and curving upwards. This plants (Table 1). The system is present in and , all of which system, which is reliant on temporally six orders of core eudicot (, are protogynous (female stage first), and reciprocal morphs, is called , , , in (), which however heterodichogamy4, in analogy to and Trochodendrales), two orders of basal is protandrous (male stage first). In the heterostyly, which is the sexual system angiosperms ( and ), second form of heterodichogamy, flowers involving reciprocal style length morphs. and in at least one monocot lineage of both morphs open simultaneously, but

http://tree.trends.com 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02280-7 596 Research Update TRENDS in Ecology & Evolution Vol.16 No.11 November 2001

Table 1. Attributes of currently known heterodichogamous flowering plants Family Plant species and Ordera Sexual system Flowerb Refs pollinating vector flower/population M–F Morphs Ratio Compatibility separation

Amaranthaceae Grayia brandegei; Caryophyllales Unisexual/ 2–3 wk Protandrous 1:1 Probably SIC 17,18 (incl. Wind monoecious versus Chenopodiaceae) protogynous Spinacia oleracea var. Caryophyllales Unisexual/ 24–48 h Protandrous 1:1 SC Cited americana; Wind dioecious (this versus in variety protogynous 18 monoecious) Annonaceae squamosa; Magnoliales Bisexual c. 12 h Protogynous, Unknown SC 21 Beetles offset by 6 h Betulaceae Corylus avellana and Fagales Unisexual/ Several daysProtandrous 1:1 SIC 6,14 other species; Wind monoecious versus protogynous Eupomatiaceae Eupomatia bennettii Magnoliales Bisexual 12–24 h Protogynous, Unknownc SC 22 and E. laurina; Beetles offset by 6 h Carya illinoensis and Fagales Unisexual/ Few days Protandrous 1:1 SC 12 probably all monoecious versus Carya spp.; Wind protogynous hindsii, Fagales Unisexual/ 1 wk Protandrous 1:1 SC 5,14, J. regia, J. cinerea monoecious versus 20 and probably all protogynous Juglans spp.; Wind Lauraceae rosaeodora Laurales Bisexual 6 or 12 h Protogynous, Unknownc Possibly SIC 15 and other species; offset by 6 h Bees Cinnamomum Laurales Bisexual 6 or 12 h Protogynous, Unknownc Possibly SIC 15 camphora and offset by 6 h C. zeylanicum; Bees guianensis and Laurales Bisexual 6 or 12 h Protogynous, Unknownc Possibly SIC 15 other species; Bees offset by 6 h thoroflora Laurales Bisexual 6 or 12 h Protogynous, Unknownc Possibly SIC 15 (incl. Clinostemon offset by 6 h maguireanum); Bees americana and Laurales Bisexual 24 h Protogynous, 1:1 Possibly SIC 23,24 P. caerulea; Bees offset by 24 h Rhamnaceae Ziziphus jujuba (1), Rosales Bisexual 12 or 21 h, Protoandrous, 1:1 SIC (species 1 25–28 Z. mauritiana (2), depending offset by 4 (unknown and 4) Z. mucronata (3), on species or 6 h in Z. spina-christi (4); species 3) Flies and bees Sapindaceae Acer pseudoplatanus, Sapindales Bisexual but 24–48 h Protandrous 1:1 to SC 11 (incl. Aceraceae) A. saccharum and functionally versus variable other species; Insects unisexual/ protogynous monoecious hirsuta; Malvales Bisexual but 8–12 d Protandrous Highly Unknown 16,19 Wind functionally versus variable unisexual/ protogynous tri-monoecious Trochodendron Trochodendrales Bisexual 10–28 d Protandrous 1:1 SC 29 aralioides; Flies versus protogynous Zingiberaceae Alpinia kwangsiensis Zingiberales Bisexual 6 h Protandrous 1:1 SC 1–3 and other species; Bees versus protogynous aAPG classification from Ref. 30. bThe male (M) and female (F) function of the flowers are separated by the times indicated, and each population comprises two reciprocal temporal morphs. SC, self-compatible; SIC, self-incompatible. cEupomatia and Cinnamomum were studied in greenhouses, and natural morph ratios are therefore unknown. For the Lauraceae canopy species studied by Kubitzki and Kurz, extremely low densities prevented the assessment of morph ratios (H. Kurz, pers. commun.).

http://tree.trends.com Research Update TRENDS in Ecology & Evolution Vol.16 No.11 November 2001 597 one morph is protogynous, the other for temporal behavioral dimorphisms in 16 Dommée, B. et al. (1990) Sexual tetramorphism in protandrous. This is the case in walnuts, plants. As they say, ignorance is no (Thymelaeaceae): evidence of the pathway from heterodichogamy to dioecy at hickories, pecans and perhaps all excuse, it is the real thing. the infraspecific level. Am. J. Bot. 77, 1449–1462 12 Juglandaceae , hazelnuts, most maples, 17 Pendleton, R.L. et al. (1988) Heterodichogamy in Grayia, Spinacia, Thymelaea, Acknowledgements Grayia brandegei (Chenopodiaceae): report from a Trochodendron and, as Li et al. now I thank Diego Medan and Rolf Borchert new family. Am. J. Bot. 75, 267–274 report1–3, Alpinia. for discussion. 18 Pendleton, R.L. et al. (2000) Gender specialization in heterodichogamous Grayia brandegei Evolutionarily, heterodichogamy is References (Chenopodiaceae): evidence for an alternative seen as coming from synchronous 1 Li, Q-J. et al. (2001) Flexible style that pathway to dioecy. Am. J. Bot. 87, 508–516 dichogamy11,13,14 and leading to encourages outcrossing. Nature 410, 432 19 Dommée, B. et al. (1995) Sexual tetramorphism in 2 Li, Q-J. et al. (2001) Study on the flexistyly dioecy8,11,13, 15–18. Phylogenetic studies Thymelaea hirsuta (Thymelaeaceae): morph ratios pollination mechanism in Alpinia plants in open-pollinated progeny. Am. J. Bot. 82, 734–740 that would test either hypothesis are not (Zingiberaceae). Acta Botanica Sinica 20 Polito, V.S. and Pinney, K. (1997) The relationship yet available. Four of the 17 genera 43, 364–369 between phenology of pistillate flower organogenesis (Acer, Grayia, Spinacia and Thymelaea) 3 Li, Q-J. et al. Stigmatic behavior and the and mode of heterodichogamy in L. contain both heterodichogamous and pollination biology of Alpinia kwangsiensis (Juglandaceae). Sex. Plant Reprod. 10, 36–39 (Zingiberaceae). Am. J. Bot. (in press) dioecious species or populations and could 21 Wester, P.J. (1910) Pollination experiments with 4 Errera, L. and Gevaert, G. (1878) Sur la structure anonas. Bull. Torrey Bot. Club 37, 529–539 be used to study the proposed pathway et les mode de fécondation des fleurs. Bull. Soc. R. 22 Endress, P.K. (1984) The flowering process in the (see data base of dioecious angiosperms Bot. Belgique 17, 38–181 Eupomatiaceae (Magnoliales). Bot. J. Syst. available at http://www.umsl.edu/ 5 Delpino, F. (1874) Ulteriori osservazioni e 104, 297–319 ~biosrenn/dioecy.pdf). considerazioni sulla dicogamia nel regno vegetale. 23 Stout, A.B. (1927) The flower behavior of Appendice. Dimorfismo nel noce (Juglans regia) e The occurrence of 1:1 morph ratios in avocados. Mem. New York Bot. Gard. 7, 145–203 pleiontismo nelle piante. Atti Soc. Ital. Sci. Nat. 24 Skutch, A.F. (1945) The behavior of the flowers of the natural populations of heterodichogamous 17, 402–407 aguacatillo (Persea caerulea). Torreya 45, 110–116 species suggests that a single pair of 6 Müller, H. (1875) Flowering of the hazel. Nature 25 Galil, J. and Zeroni, M. (1967) On the pollination alleles controls heterodichogamy. 12, 26 of Zizyphus spina–christi (L.) Willd. in Israel. Indeed, in walnuts and pecans12,14, a 7 Webb, C. (1999) Empirical studies: evolution and Israel J. Bot. 16, 71–77 maintenance of dimorphic breeding systems. In dominant–recessive mendelian factor of 26 Lyrene, P.M. (1983) Flowering and fruiting of Gender and Sexual Dimorphism in Flowering chinese jujubes in Florida. HortScience 18, 208–209 one locus and two alleles regulates Plants (Geber, M.A. et al., eds), pp. 61–95, 27 Rama Devi, K. et al. (1989) Pollination ecology of heterodichogamy. Protandry is the Springer-Verlag Zizyphus mauritiana (Rhamnaceae). Proc. Indian recessive homozygote (gg) and protogyny 8 Lloyd, D.G. and Webb, C.J. (1986) The avoidance Acad. Sci. Plant Sci. 99, 223–239 of interference between the presentation of pollen either the heterozygote (Gg) or dominant 28 Zietsman, P.C. et al. (1989) Vegetative and and stigmas in angiosperms. I. Dichogamy. New reproductive phenology of Ziziphus mucronata homozygote (GG). GG is extremely rare Zealand J. Bot. 24, 135–162 subsp. mucronata (Rhamnaceae). S. Afr. J. Bot. in nature, because heterodichogamy is 9 Cruden, R.W. (1988) Temporal dioecism: 55, 564–573 almost 100% effective at precluding systematic breadth, associated traits, and 29 Chaw, S-M. (1992) Pollination, breeding selfing12,14. By contrast, dioecy is usually temporal patterns. Bot. Gaz. 149, 1–15 syndromes, and systematics of Trochodendron 10 Bertin, R.I. and Newman, C.M. (1993) Dichogamy controlled by a pair of genes that are aralioides Sieb. & Zucc. (Trochodendraceae), a in angiosperms. Bot. Rev. 59, 112–152 relictual species in Eastern Asia. In heterogametic for males and homogametic 11 de Jong, P.C. (1976) Flowering and sex expression Phytogeography and Botanical Inventory of for females, or occasionally by three loci, in Acer L.: a biosystematic study. Meded. Taiwan (Peng, C-I., ed.), pp. 63–77, Institute of each with two alleles19. Landbouwhogeschool Wageningen 76–2, 1–201 Botany, Academia Sinica Monograph Series 12 Contrary to earlier expectations17, 12 Thompson, T.E. and Romberg, L.D. (1985) 30 APG (Angiosperm Phylogeny Group) (1998) An Inheritance of heterodichogamy in pecan. most heterodichogamous taxa are insect ordinal classification for the families of flowering J. Heredity 76, 456–458 plants. Ann. Miss. Bot. Gard. 85, 531–553 pollinated (11 versus six wind pollinated; 13 Darwin, C. (1877) The Different Forms of Flowers Table 1) and about half are self on Plants of the Same Species, Murray incompatible (Table 1). Heterodichogamy 14 Gleeson, S.K. (1982) Heterodichogamy in Susanne S. Renner depends on the exact timing of floral walnuts: inheritance and stable ratios. Evolution Dept of Biology, University of 36, 892–902 20 organogenesis and the interplay of 15 Kubitzki, K. and Kurz, H. (1984) Synchronized Missouri–St Louis, 8001 Natural Bridge Rd, environmental and genetic factors. dichogamy and dioecy in neotropical Lauraceae. St Louis, MO 63121, USA. Nothing is known about the physiological Plant Syst. Evol. 147, 253–266 e-mail: [email protected] control of flowering in the two morphs, probably because developmental events that occur only once in a season do not lend themselves to experimental analysis. If a herbaceous species were Top of the TREE! discovered in which morphs opened and closed their flowers repeatedly, then 8.76 one could do the experiments needed TREE is still the highest impact journal in to establish light-cycle control. The ecology and evolution completely unexpected discovery of heterodichogamy in Zingiberaceae1–3, (ISI Science Citation Reports, 2000) besides its intrinsic interest, should cause more biologists to be on the watch

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