Variation in Sexual Expression in the Monoecious Shrub Buxus balearica at Different Scales

Abstract

Monoecy allows high plasticity in gender expression because the production of separate female and male flowers increases the ability to respond to specific environmental circumstances. We studied variation in sexual expression and its correlates in the monoecious shrub Buxus balearica, for two years, in six populations in the Balearic Islands and four in the Iberian Peninsula. Phenotypic gender varied among populations; while island populations showed slight variations around an average gender, mainland populations showed a broad range of variation in gender among individuals, always biased towards increasing maleness compared with the other populations. Within populations, gender was not related to plant size. Between-year changes were slight and mainly consisted of an increase in relative maleness in the mast year. Reproduction did not affect gender in the next year, as assessed by either observational or experimental methods. Most variation in gender expression occurred among individuals within populations (83.6 %), followed by variation among populations (13.6 %) and years (2.8 %). Our results suggest that male-biased gender at population and plant levels was related to stressful conditions and resource limitation, because: (1) maleness was higher in mainland populations, where summer drought was stronger; (2) maleness increased with elevation; (3) fruit set was positively correlated with femaleness; (4) the percentage of male inflorescences increased over the flowering period; and (5) male inflorescences were preferentially in lower parts of the branch nodes. Higher maleness in mast years, however, could be related to increased male success under synchronic flowering.

Balearic Islands - Iberian Peninsula - monoecy - phenotypic gender - plant size - reproductive costs - spatio-temporal variation - stress.

References

• 1 Ackerly D. D., Jasienski M.. Size-dependent variation of gender in high density stands of the monoecious annual, Ambrosia artemisiifolia (Asteraceae).  Oecologia. (1990);  82 474-477
• 2 Aizen M. A., Kenigsten A.. Floral sex ratios in scrub oak (Quercus ilicifolia) vary with microtopography and stem height.  Canadian Journal of Botany. (1990);  68 1364-1368
• 3 Allison T. D.. Variation in sex expression in Canada yew (Taxus canadensis).  American Journal of Botany. (1991);  78 569-578
• 4 Arista M., Talavera S.. Gender expression in Abies pinsapo Boiss., a Mediterranean Fir.  Annals of Botany. (1997);  79 337-342
• 5 Ashman T.-L., Baker I.. Variation in floral sex allocation with time of season and currency.  Ecology. (1992);  73 1237-1243
• 6 Benedí C.. Halogaraceae-Euphorbiaceae. Castroviejo, S., Aedo, C., Benedí, C., Laínz, M., Muñoz Garmendia, F., Nieto Feliner, G., and Paiva, J., eds. Flora Iberica, Vol. 7. Madrid; CSIC, Real Jardín Botánico (1997): 1-375
• 7 Bickel A. M., Freeman D. C.. Effects of pollen vector and plant geometry on floral sex ratio in monoecious plants.  American Midland Naturalist. (1993);  130 239-247
• 8 Brunet J., Charlesworth D.. Floral sex allocation in sequentially blooming plants.  Evolution. (1995);  49 70-79
• 9 Burd M., Allen T. F. H.. Sexual allocation strategy in wind-pollinated plants.  Evolution. (1988);  42 403-407
• 10 Charnov E. L.. The Theory of Sex Allocation. Princeton; Princeton University Press (1982): 1-355
• 11 Clay K.. Size-dependent gender change in green dragon (Arisaema dracontium; Araceae).  American Journal of Botany. (1993);  80 769-777
• 12 Costich D. E.. Gender specialization across a climatic gradient: experimental comparisons of monoecious and dioecious Ecballium.  Ecology. (1995);  76 1036-1050
• 13 Delesalle V. A.. Year-to-year changes in phenotypic gender in a monoecious cucurbit, Apodanthera undulata.  American Journal of Botany. (1989);  76 30-39
• 14 Delesalle V. A., Mooreside P. D.. Estimating the costs of allocation to male and female functions in a monoecious cucurbit, Lagenaria siceraria.  Oecologia. (1995);  102 9-16
• 15 Delph L. F.. Sexual dimorphism in life history. Geber, M. A., Dawson, T. E., and Delph, L. F., eds. Gender and Sexual Dimorphism in Flowering Plants. New York; Springer Verlag (1999): 149-173
• 16 Diggle P. K.. Architectural effects and the interpretation of patterns of fruit and seed development.  Annual Review in Ecology and Systematics. (1995);  26 531-552
• 17 Dorken M. E., Barrett S. C. H.. Gender plasticity in Sagittaria sagittifolia (Alismataceae), a monoecious aquatic species.  Plant Systematics and Evolution. (2003);  237 99-106
• 18 El-Keblawy A., Lovett Doust J., Lovett Doust L., Shaltout K. H.. Labile sex expression and dynamics of gender in Thymelaea hirsuta.  Ecoscience. (1995);  2 55-66
• 19 Elle E.. Sex allocation and reproductive success in the andromonoecious perennial Solanum carolinense (Solanaceae). I. Female success.  American Journal of Botany. (1999);  86 278-286
• 20 Emms S. K.. Andromonoecy in Zigadenus paniculatus (Liliaceae): spatial and temporal patterns of sex allocation.  American Journal of Botany. (1993);  80 914-923
• 21 Fox J. F.. Size and sex allocation in monoecious woody plants.  Oecologia. (1993);  94 110-113
• 22 Freeman D. C., Harper K. T., Charnov E. L.. Sex change in plants: old and new observations and new hypotheses.  Oecologia. (1980);  47 222-232
• 23 Freeman D. C., McArthur E. D., Harper K. T.. The adaptive significance of sexual lability in plants using Atriplex canescens as a principal example.  Annals of the Missouri Botanical Garden. (1984);  71 265-277
• 24 Freeman D. C., McArthur E. D., Harper K. T., Blauer A. C.. Influence of environment on the floral sex ratio of monoecious plants.  Evolution. (1981);  35 194-197
• 25 García D., Obeso J. R., Martínez I.. Spatial concordance between seed rain and seedling establishment in bird-dispersed trees: does scale matter?.  Journal of Ecology. (2005);  93 693-704
• 26 Goldman D. A.. Minimal male/female trade-offs in Zizania palustris, a monoecious annual grass.  American Journal of Botany. (1991);  78 189-197
• 27 Jordano P.. Gender variation and expression of monoecy in Juniperus phoenicea (L.) (Cupressaceae).  Botanical Gazette. (1991);  152 476-485
• 28 Kawakita A., Kato M.. Floral biology and unique pollination system of root holoparasites, Balanophora kuroiwai and B. tobiracola (Balanophoraceae).  American Journal of Botany. (2002);  89 1164-1170
• 29 Kelly D.. The evolutionary ecology of mast seeding.  Trends in Ecology and Evolution. (1994);  9 465-470
• 30 Klinkhamer P. G. L., de Jong T. J., Metz H.. Sex and size in cosexual plants.  Trends in Ecology and Evolution. (1997);  12 260-265
• 51 Koide R. T., Robichaux R. H., Morse S. R., Smith C. M.. Plant water status, hydraulic resistance, and capacitance. Pearcy, R. W., Ehleringer, J. R., Mooney, A., and Rundel, P. W., eds. Plant Physiological Ecology. New York; Chapman and Hall (1989): 161-183
• 31 Körner C.. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems. Berlin; Springer-Verlag (1999): 1-338
• 32 Lázaro A., Traveset A.. Spatio-temporal variation in the pollination mode of Buxus balearica (Buxaceae), an ambophilous and selfing species: mainland-island comparison.  Ecography. (2005);  28 640-652
• 33 Lázaro A., Traveset A.. Reproductive success of the endangered shrub Buxus balearica Lam. (Buxaceae): pollen limitation, and inbreeding and outbreeding depression.  Plant Systematics and Evolution. (2006);  261 117-128
• 34 Lázaro A., Traveset A., Méndez M.. Masting in Buxus balearica: assessing fruiting patterns and processes at a large spatial scale.  Oikos. (2006);  115 229-240
• 35 Lloyd D. G.. Sexual strategies in plants. I. An hypothesis of sexual adjustment of maternal investment during one reproductive season.  New Phytologist. (1980 a);  86 69-79
• 36 Lloyd D. G.. Sexual strategies in plants. III. A quantitative method for describing the gender of plants.  New Zealand Journal of Botany. (1980 b);  18 103-108
• 37 Lloyd D. G., Bawa K. S.. Modification of the gender of seed plants in varying conditions.  Evolutionary Biology. (1984);  17 255-338
• 38 López-Almansa J. C., Pannell J. R., Gil L.. Female sterility in Ulmus minor (Ulmaceae): a hypothesis invoking the cost of sex in a clonal plant.  American Journal of Botany. (2003);  90 603-609
• 39 McKone M. J., Tonkyn D. W.. Intrapopulation gender variation in common ragweed (Asteraceae: Ambrosia artemisiifolia L.), a monoecious, annual herb.  Oecologia. (1986);  70 63-67
• 40 Méndez M.. Modification of phenotypic and functional gender in the monoecious Arum italicum (Araceae).  American Journal of Botany. (1998);  85 225-234
• 41 Parra-Tabla V., Rico-Gray V., Carbajal M.. Effect of defoliation on leaf growth, sexual expression and reproductive success of Cnidoscolus aconitifolius (Euphorbiaceae).  Plant Ecology. (2004);  173 153-160
• 42 Renner S. S., Ricklefs R. E.. Dioecy and its correlates in the flowering plants.  American Journal of Botany. (1995);  82 596-606
• 43 Rice W. R.. Analyzing tables of statistical tests.  Evolution. (1989);  43 223-225
• 44 Richards A. J.. Plant Breeding Systems, 2nd ed. London; Chapman and Hall (1997): 1-529
• 45 Sato T.. Size-dependent resource allocation among vegetative propagules and male and female functions in the forest herb Laportea bulbifera.  Oikos. (2002);  96 453-462
• 46 Smith C. C.. The facultative adjustment of sex ratio in lodgepole pine.  American Naturalist. (1981);  118 297-305
• 47 Sokal R. R., Rohlf F. J.. Biometry, 3rd ed. New York; W. H. Feeman and Company (1995)
• 48 Von Balthazar M., Endress P. K.. Reproductive structures and systematics of Buxaceae.  Botanical Journal of the Linnean Society. (2002);  140 193-228
• 49 Watson M. A., Casper B. B.. Morphogenetic constraints on patterns of carbon distribution in plants.  Annual Review in Ecology and Systematics. (1984);  15 233-258
• 50 Yin T., Quinn J. A.. A mechanistic model of a single hormone regulating both sexes in flowering plants.  Bulletin of the Torrey Botanical Club. (1992);  119 431-441

Editor: J. T. M. Elzenga