Plant Ecology

, Volume 218, Issue 10, pp 1163–1170 | Cite as

Lack of trade-offs between the male and female sexual functions in the gynodioecious herb Geranium sylvaticum

  • Sandra VargaEmail author
  • Minna-Maarit Kytöviita


Resource allocation trade-offs between sexual functions are predicted, but these are usually measured only at the whole plant level. In some gynodioecious species, individuals with partially restored male fertility exist providing an opportunity to investigate whether the costs associated with male fertility restoration are linked to seed production. In this study, we examined whether there is a relationship between the numbers of stamens and seeds produced both at the flower level and at the plant level in the gynodioecious herb Geranium sylvaticum. We individually marked flowers in plants varying in the degree of male sterility in the field and counted the number of seeds produced. There was no significant correlation between the numbers of stamens and seeds produced at the flower level suggesting an absence of resource trade-off between female and male functions. Furthermore, the numbers of stamens and seeds were positively correlated at the plant level. The lack of trade-offs between the two sexual functions in this species indicates that relative sex allocation was not affected by resources within a single season and/or that the male costs were relatively small.


Gynodioecy Male fertility restoration Resource sex allocation Seed and stamen number 



We thank Anna Nieminen and Janne Ruuth for helping us with the practical work. This study was financially supported by the Academy of Finland (SV).


  1. Ashman T-L (1999) Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. J Evol Biol 12:648–661CrossRefGoogle Scholar
  2. Ashman T-L, Majetic CJ (2006) Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96:343–352CrossRefPubMedGoogle Scholar
  3. Ashman T-L, Pacyna J, Diefenderfer C, Leftwich T (2001) Size-dependent sex allocation in a gynodioecious wild strawberry: the effects of sex morph and inflorescence architecture. Int J Plant Sci 162:327–334CrossRefGoogle Scholar
  4. Asikainen E (2004) Maintenance of gynodioecy in Geranium sylvaticum. Dissertation, Turku UniversityGoogle Scholar
  5. Asikainen E, Mutikainen P (2003) Female frequency and relative fitness of females and hermaphrodites in gynodioecious Geranium sylvaticum (Geraniaceae). Am J Bot 90:226–234CrossRefPubMedGoogle Scholar
  6. Asikainen E, Mutikainen P (2005a) Preferences of pollinators and herbivores in gynodioecious Geranium sylvaticum. Ann Bot 95:879–886CrossRefPubMedPubMedCentralGoogle Scholar
  7. Asikainen E, Mutikainen P (2005b) Pollen and resource limitation in a gynodioecious species. Am J Bot 92:487–494CrossRefPubMedGoogle Scholar
  8. Atlan A, Gouyon PH, Fournial T et al (1992) Sex allocation in an hermaphroditic plant: the case of gynodioecy in Thymus vulgaris L. J Evol Biol 5:189–203CrossRefGoogle Scholar
  9. Bailey MF (2002) A cost of restoration of male fertility in a gynodioecious species, Lobelia siphilitica. Evolution 56:2178–2186CrossRefPubMedGoogle Scholar
  10. Bazzaz F, Grace J (1997) Plant resource allocation. Academic Press, San DiegoGoogle Scholar
  11. Caruso CM, Case AL, Bailey MF (2012) The evolutionary ecology of cytonuclear interactions in angiosperms. Trends Plant Sci 17:638–643CrossRefPubMedGoogle Scholar
  12. Cody ML (1966) A general theory on clutch size. Evolution 20:174–184CrossRefPubMedGoogle Scholar
  13. Couvet D, Ronce O, Gliddon C (1998) The maintenance of nucleocytoplasmic polymorphism in a metapopulation: the case of gynodioecy. Am Nat 152:59–70CrossRefPubMedGoogle Scholar
  14. De Haan AA, Hundscheid MPJ, Van Hinsberg A (1997) Effects of CMS types and restorer alleles on plant performance in Plantago lanceolata L.: an indication for cost of restoration. J Evol Biol 10:803–820CrossRefGoogle Scholar
  15. del Castillo RF, Trujillo S (2009) Evidence of restoration cost in the annual gynodioecious Phacelia dubia. J Evol Biol 22:306–313CrossRefPubMedGoogle Scholar
  16. Devlin B (1989) Components of seed and pollen yield of Lobelia cardinalis: variation and correlations. Am J Bot 76:204CrossRefGoogle Scholar
  17. Dudash MR (1991) Plant size effects on female and male function in hermaphroditic Sabatia angularis (Gentianaceae). Ecology 72:1004–1012CrossRefGoogle Scholar
  18. Dufaÿ M, Vaudey V, de Cauwer I et al (2008) Variation in pollen production and pollen viability in natural populations of gynodioecious Beta vulgaris ssp. maritima: evidence for a cost of restoration of male function? J Evol Biol 21:202–212PubMedGoogle Scholar
  19. Elzinga JA, Varga S (2017) Prolonged stigma and flower lifespan in females of the gynodioecious plant Geranium sylvaticum. Flora 226:72–81CrossRefGoogle Scholar
  20. Johnson MTJ, deWitt Smith S, Rausher MD (2010) Effects of plant sex on range distributions and allocation to reproduction. New Phytol 186:769–779CrossRefPubMedGoogle Scholar
  21. Klinkhamer PGL, de Jong TJ, Nell HW (1994) Limiting factors for seed production and phenotypic gender in the gynodioecious species Echium vulgare (Boraginaceae). Oikos 71:469CrossRefGoogle Scholar
  22. Koelewijn HP (2003) Variation in restorer genes and primary sexual investment in gynodioecious Plantago coronopus: the trade-off between male and female function. Proc Royal Soc B 270:1939–1945CrossRefGoogle Scholar
  23. Koelewijn HP, Hunscheid M (2000) Intraspecific variation in sex allocation in hermaphroditic Plantago coronopus (L.). J Evol Biol 13:302–315CrossRefGoogle Scholar
  24. Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
  25. Lloyd DG (1980) Sexual strategies in plants III. A quantitative method for describing the gender of plants. New Zeal J Bot 18:103–108CrossRefGoogle Scholar
  26. Maurice S, Charlesworth D, Desfeux C et al (1993) The evolution of gender in hermaphrodites of gynodioecious populations with nucleo-cytoplasmic male-sterility. Proc Royal Soc B 251:253–261CrossRefGoogle Scholar
  27. Maurice S, Belhassen E, Couvet D, Gouyon P-H (1994) Evolution of dioecy: can nuclear-cytoplasmic interactions select for maleness? Heredity 73:346–354CrossRefPubMedGoogle Scholar
  28. Méndez M, Traveset A (2003) Sexual allocation in single-flowered hermaphroditic individuals in relation to plant and flower size. Oecologia 137:69–75CrossRefPubMedGoogle Scholar
  29. Mossop R, Macnair MR, Robertson AW (1994) Within-population variation in sexual resource allocation in Mimulus guttatus. Func Ecol 8:410CrossRefGoogle Scholar
  30. Obeso J-R (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  31. Parachnowitsch AL, Elle E (2004) Variation in sex allocation and male–female trade-offs in six populations of Collinsia parviflora (Scrophulariaceae s.l.). Am J Bot 91:1200–1207CrossRefPubMedGoogle Scholar
  32. Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596CrossRefPubMedGoogle Scholar
  33. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267CrossRefGoogle Scholar
  34. Rivkin LR, Case AL, Caruso CM (2016) Why is gynodioecy a rare but widely distributed sexual system? lessons from the Lamiaceae. New Phytol 211:688–696CrossRefPubMedGoogle Scholar
  35. Ross M (1990) Sexual asymmetry in hermaphroditic plants. Trends Ecol Evol 5:43–47CrossRefPubMedGoogle Scholar
  36. Sato H, Yahara T (1999) Trade-offs between flower number and investment to a flower in selfing and outcrossing varieties of Impatiens hypophylla (Balsaminaceae). Am J Bot 86:1699–1707CrossRefPubMedGoogle Scholar
  37. Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180CrossRefGoogle Scholar
  38. Schultz ST (1994) Nucleo-cytoplasmic male sterility and alternative routes to dioecy. Evolution 48:1933–1945CrossRefPubMedGoogle Scholar
  39. Stearns SC (1989) Trade-offs in life-history evolution. Func Ecol 3:259–268Google Scholar
  40. Vaarama A, Jääskeläinen O (1967) Studies on gynodioecism in the Finnish populations of Geranium silvaticum L. Ann Aca Sci Fenn B 108:1–39Google Scholar
  41. Varga S (2014) Pre-dispersal seed predation in gynodioecious Geranium sylvaticum is not affected by plant gender or flowering phenology. Arthropod Plant Interac 8:253–260Google Scholar
  42. Varga S, Kytöviita M-M (2010) Gender dimorphism and mycorrhizal symbiosis affect floral visitors and reproductive output in Geranium sylvaticum. Func Ecol 24:750–758CrossRefGoogle Scholar
  43. Varga S, Kytöviita M-M (2016) Light availability affects sex lability in a gynodioecious plant. Am J Bot 103:1928–1936CrossRefPubMedGoogle Scholar
  44. Varga S, Nuortila C, Kytöviita M-M (2013a) Nectar sugar production across floral phases in the gynodioecious protandrous plant Geranium sylvaticum. PLoS ONE 8:e62575CrossRefPubMedPubMedCentralGoogle Scholar
  45. Varga S, Vega-Frutis R, Kytöviita M-M (2013b) Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. New Phytol 199:812–821CrossRefPubMedGoogle Scholar
  46. Varga S, Laaksonen E, Siikamäki P, Kytöviita M-M (2015) Absence of sex differential plasticity to light availability during seed maturation in Geranium sylvaticum. PLoS ONE 10:e0118981CrossRefPubMedPubMedCentralGoogle Scholar
  47. Volkova PA, Rudakova VS, Shipunov AB (2007) Sex ratios in populations of Geranium sylvaticum in European Russia. Plant Spec Biol 22:125–128CrossRefGoogle Scholar
  48. Whitton J, Sears CJ, Baack EJ, Otto SP (2008) The dynamic nature of apomixis in the angiosperms. Int J Plant Sci 169:169–182CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Joseph Banks Laboratories, School of Life SciencesUniversity of LincolnLincolnUK
  2. 2.Department of Biological and Environmental ScienceUniversity of JyvaskylaJyvaskylaFinland

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