Skip to main content
SpringerLink
Log in

Sexual allocation in the gynodioecious species Cyananthus macrocalyx (Campanulaceae) at high elevations in the Sino-Himalaya Mountains

  • Original Article
  • Published:
Alpine Botany Aims and scope Submit manuscript

Abstract

Sexual allocation pattern is considered highly relevant for the maintenance of females in the process of evolution from hermaphrodites to dioecy. Theoretical and empirical studies predict that gynodioecious plants should invest more resources in male function under harsher environments and/or when female frequency is higher; and that there are trade-offs between male and female function. We studied sexual allocation pattern in the gynodioecious species Cyananthus macrocalyx in two populations in SW China. The results showed that although the total flower mass in hermaphrodites was significantly higher than that in females, females and hermaphrodites allocated similar biomass to female function (pistil biomass). As a consequence, females allocated relatively more resource to female function, while hermaphrodites allocated relatively more resource to pollinator attractiveness. There was no difference in total flower mass, pistil mass, and pollen production in hermaphrodites between the two populations. These results suggest that the females compensate for the disadvantage of lacking male function by allocating relatively more resource to female function, while hermaphrodites gain fitness through both male and female functions. This study supports the idea that if females are to be maintained in a gynodioecious population, they must allocate more resource to female functions than is necessary for hermaphrodites. However, our results were in contrast to those of previous studies, in that trade-offs between male and female functions and male-biased allocation under high female frequency were not observed. This study adds to the body of research on plant sexual allocation, and for that it is, at least at some aspects, contrary to previous statements, it could be helpful for advancing the theoretical predictions in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alonso C, Herrera CM (2011) Back-and-forth hermaphroditism: phylogenetic context of reproductive system evolution in subdioecious Daphne laureola. Evol Dev 65:1680–1692

    Article  Google Scholar 

  • Arnan X, Escola A, Rodrigo A, Bosch J (2014) Female reproductive success in gynodioecious Thymus vulgaris: pollen versus nutrient limitation and pollinator foraging behaviour. Bot J Linnean Soc 175:395–408

    Article  Google Scholar 

  • Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate andes of central Chile. 1. Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97

    Article  Google Scholar 

  • Ashman TL (1994) Reproductive allocation in hermaphrodite and female plants of Sidalcea oreganas sp. spicata (Malvaceae) using 4 currencies. Am J Bot 81:433–438

    Article  Google Scholar 

  • Ashman TL (1999) Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. J Evol Biol 12:648–661

    Article  Google Scholar 

  • Ashman TL, Baker I (1992) Variation in floral sex allocation with time of season and currency. Ecology 73:1237–1243

    Article  Google Scholar 

  • Ashman TL, Stanton M (1991) Seasonal-variation in pollination dynamics of sexually dimorphic Sidalcea-oreganas sp. spicata (Malvaceae). Ecology 72:993–1003

    Article  Google Scholar 

  • Baker AM, Burd M, Climie KM (2005) Flowering phenology and sexual allocation in single-mutation lineages of Arabidopsis thaliana. Evolution 59:970–978

    Article  PubMed  Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  PubMed  Google Scholar 

  • Bawa KS, Opler (1975) Dioecism in tropical tress. Evolution 29:167–179

    Article  Google Scholar 

  • Bawa KS (1980) Evolution of dioecy in flowering plants. Annu Rev Ecol Syst 11:15–39

    Article  Google Scholar 

  • Bazzaz FA, Reekie EG (1985) The meaning and measurement of reproductive effort in plants. In: White J (ed) Studies in Plant Demography: A festschrift for John L Harper. Academic Press, London, pp 373–387

    Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392

    Article  Google Scholar 

  • Burd M, Head G (1992) Phenological aspects of male and female function in hermaphroditic plants. Am Nat 140:305–324

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1981) Allocation of resources to male and female functions in hermaphrodites. Biol J Linnean Soc 15:57–74

    Article  Google Scholar 

  • Charlesworth D, Morgan MT (1991) Allocation of resources to sex functions in flowering plants. Philos Trans R Soc B-Biol Sci 332:91–102

    Article  Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Chen JG, Yang Y, Zhang ZQ, Niu Y, Sun H (2013) A nodding capitulum enhances the reproductive success of Cremanthodium campanulatum (Asteraceae) at high elevations in the Sino-Himalayan Mountains. Plant Ecol Divers 6:487–494

    Article  Google Scholar 

  • Cruden RW (1977) Pollen-ovule ratios—conservative indicator of breeding systems in flowering plants. Evolution 31:32–46

    Article  Google Scholar 

  • Cruden RW (2000) Pollen grains: why so many? Plant Syst Evol 222:143–165

    Article  Google Scholar 

  • Darwin CR (1877) The different forms of flowers on plants of the same species. John Murray, London, p 279

    Book  Google Scholar 

  • Delph LF (1996) Flower size dimorphism in plants with unisexual flowers. In: Lloyd D, Barrett S (eds) Floral biology: studies on floral evolution in animal pollinated plants. Springer, US, pp 217–237

  • Delph LF (2009) Sex allocation: evolution to and from dioecy. Curr Biol 19:R249–R251

    Article  CAS  PubMed  Google Scholar 

  • Delph LF, Lloyd DG (1991) Environmental and genetic-control of gender in the dimorphic shrub hebe-subalpina. Evolution 45:1957–1964

    Article  Google Scholar 

  • Delph LF, Wolf DE (2005) Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytol 166:119–128

    Article  PubMed  Google Scholar 

  • Dorken ME, Mitchard ETA (2008) Phenotypic plasticity of hermaphrodite sex allocation promotes the evolution of separate sexes: an experimental test of the sex-differential plasticity hypothesis using Sagittaria latifolia (alismataceae). Evolution 62:971–978

    Article  PubMed  Google Scholar 

  • Duan YW, Zhang TF, Liu JQ (2007) Interannual fluctuations in floral longevity, pollinator visitation and pollination limitation of an alpine plant (Gentiana straminea Maxim., Gentianaceae) at two elevations in the Qinghai-Tibetan Plateau. Plant Syst Evol 267:255–265

    Article  Google Scholar 

  • Eckhart VM (1992) Resource compensation and the evolution of gynodioecy in Phacelia-Linearis (Hydrophyllaceae). Evolution 46:1313–1328

    Article  Google Scholar 

  • Ehlers BK, Thompson JD (2004) Temporal variation in sex allocation in hermaphrodites of gynodioecious Thymus vulgaris L. J Ecol 92:15–23

    Article  Google Scholar 

  • Gedroc JJ, Mcconnaughay KDM, Coleman JS (1996) Plasticity in root/shoot partitioning: optimal, ontogenetic, or both? Funct Ecol 10:44–50

    Article  Google Scholar 

  • Goldman DA, Willson MF (1986) Sex allocation in functionally hermaphroditic plants—a review and critique. Bot Rev 52:157–194

    Article  Google Scholar 

  • Ishii HS, Harder LD (2012) Phenological associations of within- and among-plant variation in gender with floral morphology and integration in protandrous Delphinium glaucum. J Ecol 100:1029–1038

    Article  Google Scholar 

  • Koelewijn HP, Hunscheid MPH (2000) Intraspecific variation in sex allocation in hermaphroditic Plantago coronopus (L.). J Evol Biol 13:302–315

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Leigh A, Cosgrove MJ, Nicotra AB (2006) Reproductive allocation in a gender dimorphic shrub: anomalous female investment in Gynatrix pulchella? J Ecol 94:1261–1271

    Article  Google Scholar 

  • Levins R (1968) Evolution in changing environments. Princeton University Press, USA

  • Liu JQ, Duan YW, Hao G, Ge XJ, Sun H (2014) Evolutionary history and underlying adaptation of alpine plants on the Qinghai-Tibet Plateau. J Syst Evol 52:241–249

    Article  Google Scholar 

  • Lloyd DG (1976) The transmission of genes via pollen and ovules in gynodioecious angiosperms. Theor Popul Biol 9:299–316

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Luo YB, Huang SQ (2012) Effects of soil moisture and floral herbivory on sexual expression in a gynodioecious orchid. J Syst Evol 50:454–459

    Article  Google Scholar 

  • Mazer SJ, Delesalle VA, Neal PR (1999) Responses of floral traits to selection on primary sexual investment in Spergularia marina: the battle between the sexes. Evolution 53:717–731

    Article  Google Scholar 

  • Mittermeier RA, Myers N, Mittermeier CG, Gil PR (1999) Hot spots: earth’s biologically richest and most endangered terrestrial ecoregions. Cemex, Conservation Int, Mexico City

  • McCauley DE, Brock MT (1998) Frequency-dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution 52:30–36

    Article  Google Scholar 

  • Medan D, Montaldo NH, Devoto M, Mantese A, Vasellati V, Roitman GG, Bartoloni NH (2002) Plant-pollinator relationships at two altitudes in the Andes of Mendoza, Argentina. Arct Antarct Alp Res 34:233–241

    Article  Google Scholar 

  • Niu Y, Yang Y, Zhang ZQ, Li ZM, Sun H (2011) Floral closure induced by pollination in gynodioecious Cyananthus delavayi (Campanulaceae): effects of pollen load and type, floral morph and fitness consequences. Ann Bot 108:1257–1268

    Article  PubMed  PubMed Central  Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Pannell JR, Eppley SM, Dorken ME, Berjano R (2014) Regional variation in sex ratios and sex allocation in androdioecious Mercurialis annua. J Evol Biol 27:1467–1477

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50

    Article  CAS  PubMed  Google Scholar 

  • Ramsey M, Vaughton G, Peakall R (2006) Does inbreeding avoidance maintain gender dimorphism in Wurmbea dioica (Colchicaceae)? J Evol Biol 19:1497–1506

    Article  CAS  PubMed  Google Scholar 

  • Ramula S, Mutikainen P (2003) Sex allocation of females and hermaphrodites in the gynodioecious Geranium sylvaticum. Ann Bot 92:207–213

    Article  PubMed  PubMed Central  Google Scholar 

  • Reekie EG, Bazzaz FA (2005) Reproductive Allocation in Plants. Elsevier, Amsterdam

    Google Scholar 

  • Sakai AK, Weller SG, Chen ML, Chou SY, Tasanont C (1997) Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51:724–736

    Article  Google Scholar 

  • Schoen DJ (1982) Male reproductive effort and breeding system in an hermaphroditic plant. Oecologia 53:255–257

    Article  Google Scholar 

  • Song B, Zhang ZQ, Stöcklin J, Yang Y, Niu Y, Chen JG, Sun H (2013) Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 72:359–370

    Article  Google Scholar 

  • Vaughton G, Ramsey M (2002) Evidence of gynodioecy and sex ratio variation in Wurmbea biglandulosa (Colchicaceae). Plant Syst Evol 232:167–179

    Article  Google Scholar 

  • Williams CF, Kuchenreuther MA, Drew A (2000) Floral dimorphism, pollination, and self-fertilization in gynodioecious Geranium richardsonii (Geraniaceae). Am J Bot 87:661–669

    Article  CAS  PubMed  Google Scholar 

  • Wu YR, He W, Wang SF (1988) Species and Distribution. Beesfrom Yunnan (Hymenoptera: Apidae). Yunnan Science and Technology Press, Kunming, pp 1–8

    Google Scholar 

  • Zhang YW, Wang Y, Yu Q, Zhao JM (2008) Sex expression, female frequency, and reproductive output in a gynodioecious clonal herb, Glechoma longituba (Lamiaceae). Plant Ecol 199:255–264

    Article  Google Scholar 

  • Zhang DC, Zhang YH, Boufford DE, Sun H (2009) Elevational patterns of species richness and endemism for some important taxa in the Hengduan Mountains, Southwestern China. Biodivers Conserv 18:699–716

    Article  Google Scholar 

Download references

Acknowledgments

We thank Yi XJ, Sha W, and Meng JX for their assistance in data collection. We thank two anonymous reviewers for helpful comments on previous versions of the manuscript and Joelle Hoggan for English editing of this paper. This work was supported by grants from Strategic Priority Research Program (B) of the Chinese Academy of Sciences (Grant No. XDB03030112), the Natural Science Foundation of China (NSFC) (Grant No. U1136601 to H Sun, 31470321, 31270005 to Y Yang).

Author information

Authors and Affiliations

  1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, People’s Republic of China

    Jian-Guo Chen, Yang Niu, Yang Yang & Hang Sun

Authors
  1. Jian-Guo Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yang Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yang Yang or Hang Sun.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, JG., Niu, Y., Yang, Y. et al. Sexual allocation in the gynodioecious species Cyananthus macrocalyx (Campanulaceae) at high elevations in the Sino-Himalaya Mountains. Alp Botany 126, 49–57 (2016). https://doi.org/10.1007/s00035-015-0154-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-015-0154-2

Keywords

Search

Navigation