Skip to main content
SpringerLink
Log in

Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis

  • Review
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Female fecundity advantage in gynodioecious plants is required for the spread and maintenance of this reproductive system. However, not all reproductive characters show female advantage in all species. We used a meta-analysis to summarise differences between females and hermaphrodites reported from the literature for several reproductive traits. Further we tested three hypotheses, (1) that female plants of species with many ovules produce more seeds per fruit while those with few ovules produce heavier seeds, (2) that females are more pollen limited than hermaphrodites, and (3) that floral sexual size dimorphism is more pronounced in species with few ovules, either because female reproductive success is less limited by pollen availability in such species or because flowers with few ovules require a smaller floral structure to protect the carpels. Overall, females compared to hermaphrodites produced more but smaller flowers, had higher fruit set, higher total seed production, and produced heavier seeds that germinated better. Species with many versus few ovules differed in female advantage for flower size dimorphism, flower number, fruit set and total seed production. However seed size, seed set per fruit and seed germination differences between females and hermaphrodites did not differ significantly between species with few and many ovules. We also found no evidence for differential pollen limitation between females and hermaphrodites. Degree of floral sexual size dimorphism differed significantly between species with few and many ovules. Though pistillate flowers were generally smaller than those of hermaphrodites, species with many ovules showed less difference in flower size between the sexes, suggesting either that the protective role of the perianth constrains the evolution of sexual size dimorphism in species with many ovules or that selection for adequate pollination in species with many ovules impedes the reduction in flower size of females.

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.

Similar content being viewed by others

References

  • Ågren J, Willson MF (1991) Gender variation and sexual differences in reproductive characters and seed production in gynodioecious Geranium maculatum. Am J Bot 78:470–480

    Google Scholar 

  • Alonso C, Herrera CM (2001) Neither vegetative nor reproductive advantages account for high frequency of male-steriles in southern Spanish gynodioecious Daphne laureola (Thymelaeaceae). Am J Bot 88:1016–1024

    PubMed  Google Scholar 

  • Arnqvist G, Wooster D (1995) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10:236–240

    Article  Google Scholar 

  • Arroyo MTK, Raven PH (1975) The evolution of subdioecy in morphologically gynodioecious species of Fuchsia sect. encliandra (Onagraceae). Evolution 29:500–511

    Google Scholar 

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

    Article  Google Scholar 

  • Ashman T-L (1999b) Quantitative genetics of floral traits in a gynodioecious wild strawberry Fragaria virginiana: implications for the independent evolution of female and hermaphrodite floral phenotypes. Heredity 83:733–741

    Article  PubMed  Google Scholar 

  • Ashman T-L (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81:2577–2591

    Google Scholar 

  • Ashman T-L, Stanton M (1991) Seasonal variation in pollination dynamics of sexually imorphic Sidalcea oregana ssp. spicata (Malvaceae). Ecology 72:993–1003

    Google Scholar 

  • Bell G (1985) On the function of flowers. Proc R Soc Lond B 224:223–265

    Google Scholar 

  • Carrol SB, Delph LF (1996) The effects of gender and plant architecture on allocation to flowers in dioecious Silene latifolia (Caryophyllaceae). Int J Plant Sci 157:493–500

    Article  Google Scholar 

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

    Google Scholar 

  • Charlesworth D, Laporte V (1998) The male-sterility polymorphism of Silene vulgaris: analysis of genetic data from two populations and comparison with Thymus vulgaris. Genetics 150:1267–1282

    CAS  PubMed  Google Scholar 

  • Collin CL, Pennings PS, Rueffler C, Widmer A, Shykoff JA (2002) Natural enemies and sex: how seed predators and pathogens contribute to sex-differential reproductive success in a gynodioecious plant. Oecologia 131:94–102

    Google Scholar 

  • Connor HE (1965) Breeding system in New Zealand grasses. VI. Control of gynodioecism in Cortaderia richardii (Endl) Zotov. N Z J Bot 3:233–242

    Google Scholar 

  • Connor HE (1973) Breeding system in Cortaderia (Graminae). Evolution 27:663–678

    Google Scholar 

  • Connor HE (1990) Breeding system in New Zealand grasses. XI. Gynodioecism in Chionochloa bromoides. N Z J Bot 28:59–65

    Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. Murray, London

  • Del Castillo RF (1993) Consequences of male sterility in Phacelia dubia. Evol Trends Plants 7:15–22

    Google Scholar 

  • Delph LF (1996) Flower size dimorphism in plants with unisexual flowers. In: Lloyd DG, Barret SCH (eds) Floral biology. Studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 217–237

  • Delph LF, Carroll SB (2001) Factors affecting relative seed fitness and female frequency in a gynodioecious species, Silene acaulis. Evol Ecol Res 3:487–505

    Google Scholar 

  • Delph LF, Lively CM (1992) Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63:161–170

    Google Scholar 

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

    Google Scholar 

  • Delph LF, Galloway LF, Stanton ML (1996) Sexual dimorphism in flower size. Am Nat 148:299–320

    Article  Google Scholar 

  • Delph LF, Bailey MF, Marr DL (1999) Seed provisioning in gynodioecious Silene acaulis (Caryophyllaceae). Am J Bot 86:140–144

    Google Scholar 

  • Desfeux C, Maurice S, Henry J-P, Lejeune B, Gouyon P-H (1996) Evolution of the reproductive systems in the genus Silene. Proc R Soc Lond Ser B 263:409–414

    Google Scholar 

  • Dinnetz P, Jerling L (1997) Gynodioecy in Plantago maritima L.; no compensation for loss of male function. Acta Bot Neerl 46:193–206

    Google Scholar 

  • Dudle D (1999) Maintenance and consequences of females in the gynodioecious plant Lobelia siphilitica. PhD thesis. Indiana University, Ind.

  • Dulberger R, Horovitz A (1984) Gender polymorphism in flowers of Silene vulgaris (Moench) Garcke (Caryophyllaceae). Bot J Linn Soc 89:101–117

    Google Scholar 

  • Eckhart VM (1992) The genetics of gender and the effects of gender on floral characters in gynodioecious Phacelia linearis (Hydrophyllaceae). Am J Bot 79:792–800

    Google Scholar 

  • Eckhart VM (1999) Sexual dimorphism in flowers adn inflorescences. In: Geber M, Dawson T, Delph L (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin Heidelberg New York, pp 123–148

  • Garcia-Franco JG, Arroyo MTK (1995) Breeding system, sex ratio and individual size of the gynodioecious Nototriche compacta (Malvaceae) in the Andes of central Chile. Plant Species Biol 10:147–153

    Google Scholar 

  • Gigord L, Lavigne C, Shykoff JA, Atlan A (1999) Evidence for effects of restorer genes on male and female reproductive functions of hermaphrodites in the gynodioecious species Thymus vulgaris L. J Evol Biol 12:596–604

    Article  Google Scholar 

  • Giles BE (1990) The effects of variation in seed size on growth and reproduction in the wild barley Hordeum vulgare ssp spontaneum. Heredity 64:239–250

    Google Scholar 

  • Gouyon P-H, Vichot F, van Damme JMM (1991) Nuclear-cytoplasmic male sterility: Single point equilibria versus limit cycles. Am Nat 137:498–514

    Article  Google Scholar 

  • Graff A (1999) Population sex structure and reproductive fitness in gynodioecious Sidalcea malviflora malviflora (Malvaceae). Evolution 53:1714–1722

    Google Scholar 

  • Guitián P, Medrano M (2000) Sex expression and fruit set in Silene littorea (Caryophyllaceae): variation among populations. Nord J Bot 20:467–473

    Google Scholar 

  • Hermanutz LA, Innes DJ (1994) Gender variation in Silene acaulis (Caryophyllaceae). Plant Syst Evol 191:69–81

    Google Scholar 

  • Jolls CL, Chenier TC (1989) Gynodioecy in Silene vulgaris (Caryophyllaceaea): progeny success, experimental design, and maternal effects. Am J Bot 76:1360–1367

    Google Scholar 

  • Jordano P (1993) Pollination biology of Prunus mahaleb L.: deferred consequences of gender variation for fecundity and seed size. Biol J Linn Soc 50:65–84

    Article  Google Scholar 

  • Jürgens A, Witt T, Gottsberger G (1996) Reproduction and pollination in central European populations of Silene and Saponaria species. Bot Acta 109:316–324

    Google Scholar 

  • Kawakubo N (1994) Gynodioecy in Cirsium chikushiense Koidz. (Compositae). Ann Bot 74:357–364

    Article  Google Scholar 

  • Kesseli R, Jain SK (1984) An ecological genetic study of gynodioecy in Limnanthes douglasii (Limnanthaceae). Am J Bot 71:775–786

    Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Wesselingh RA (1991) Implications of differences between hermaphrodite and female flowers for attractiveness to pollinators and seed production. Neth J Zool 41:130–143

    Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Nell HW (1994) Limiting factors for seed production and phenotypic gender in the gynodioecious species Echium vulgare (Boraginaceae). Oikos 71:469–478

    Google Scholar 

  • Koelewijn HP (1996) Sexual differences in reproductive characters in gynodioecious Plantago coronopus. Oikos 75:443–452

    Google Scholar 

  • Lewis D (1941) Male sterility in natural populations of hermaphrodite plants. New Phytol 40:56–63

    Google Scholar 

  • Lloyd DG, Webb CJ, Primack RB (1980) Sexual strategies in plants. II. Data on temporal regulation of maternal investment. New Phytol 86:81–92

    Google Scholar 

  • Maki M (1993) Outcrossing and fecundity advantage of females in gynodioecious Chionographis japonica var. kurohimensis (Liliaceae). Am J Bot 80:629-634

    Google Scholar 

  • Maki M (1996) Differences in plant size and flower production between hermaphrodites and females of two gynodioecious Chionographis (Liliaceae). Can J Bot 74:150–153

    Google Scholar 

  • Marshall M (1997) The maintenance of gynodioecy in Sidalcea hendersonii. Master's thesis. University of British Columbia

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

    Google Scholar 

  • McCauley DE, Taylor D (1997) Local population structure and sex ratio: evolution in gynodioecious plants. Am Nat 150:406–419

    Article  Google Scholar 

  • Molina-Freaner F, Jain SK (1992) Female frequencies and fitness components between sex phenotypes among gynodioecious populations of the colonizing species Trifolium hirtum All. in California. Oecologia 92:279–286

    Google Scholar 

  • Philipp M (1980) Reproductive biology of Stellaria longipes Goldie as revealed by a cultivation experiment. New Phytol 85:557–569

    Google Scholar 

  • Plack A (1957) Sexual dimorphism in Labiatae. Nature 180:1218–1219

    Google Scholar 

  • Puterbaugh MN, Weid A, Galen C (1997) The functional ecology of gynodioecy in Eritrichum aretioides (Boraginaceae), the alpine forget-me-not. Am J Bot 84:393–400

    Google Scholar 

  • Queller DC (1983) Sexual selection in hermaphrodite plants. Nature 305:706–707

    Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis with resampling tests. Sinauer, Sunderland, Mass.

    Google Scholar 

  • Sakai AK, Weller SG, Chen M-L, Chou S-Y, Tasanont C (1997) Evolution of gynodioecy and maintenance of females: The role of inbreeding depression, outcrossing rates, and resource allocation in Scheidea adamantis (Caryophyllaceae). Evolution 51:724–736

    Google Scholar 

  • Shykoff JA (1988) Maintenance of gynodioecy in Silene acaulis (Caryophyllaceae): stage-specific fecundity and viability selection. Am J Bot 75:844–850

    Google Scholar 

  • Shykoff JA (1992) Sex polymorphism in Silene acaulis (Caryophyllaceae) and the possible role of sexual selection in maintaining females. Am J Bot 79:138–143

    Google Scholar 

  • Shykoff JA, Bucheli E, Kaltz O (1997) Anther smut disease in Dianthus silvester (Caryophyllaceae): natural selection on floral traits. Evolution 51:383–392

    Google Scholar 

  • Stevens DP (1988) On the gynodioecious polymorphism in Saxifraga granulata L. (Saxifragaceae). Biol J Linn Soc 35:15–28

    Google Scholar 

  • Stevens DP, Richards AJ (1985) Gynodioecy in Saxifraga granulata L. (Saxifragaceae). Plant Syst Evol 151:43–54

    Google Scholar 

  • Steyn EMA, Robbertse PJ (1990) Fruit production in a morphologically gynodioecious population of Bequaertiodendron magalismontanum. S Afr J Bot 56:6–10

    Google Scholar 

  • Sugawara T (1993) Sexual polymorphism in Moehringia lateriflora (Caryophyllaceae). Acta Phytotaxon Geobot 44:3–10

    Google Scholar 

  • Sugawara T, Horii Y (1995) Sexual dimorphism in Arenaria merckioides var chokaiensis (Caryophyllaceae). Acta Phytotaxon Geobot 46:47–53

    Google Scholar 

  • Sugawara T, Nakamura A, Kanbayashi M, Hoshi H, Mikami M (1994) Floral and reproductive biology of gynodioecious Dianthus superbus L. var superbus (Caryophyllaceae). Acta Phytotaxon Geobot 45:23–31

    Google Scholar 

  • Talavera S, Arista M, Salgueiro FJ (1996) Population size, pollination and breeding system of Silene stockenii Chater (Caryophyllaceae), an annual gynodioecious species of southern Spain. Bot Acta 109:333–339

    Google Scholar 

  • Uno GE (1982) Comparative reproductive biology of hermaphroditic and male-sterile Iris douglasiana Herb. (Iridaceae). Am J Bot 69:818–823

    Google Scholar 

  • Widén M (1992) Sexual reproduction in a clonal gynodioecious herb Glechoma hederacea. Oikos 63:430–438

    Google Scholar 

  • Widén B, Widén M (1990) Pollen limitation and distance-dependent fecundity in females of the clonal gynodioecious herb Glechoma hederacea (Lamiaceae). Oecologia 83:191–196

    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

    PubMed  Google Scholar 

  • Wolfe LM, Schmida A (1997) The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78:101–110

    Google Scholar 

Download references

Acknowledgements

The authors thank C. Alonso, D. Charlesworth, D. Dudle, C.M. Herrera, L. Lafuma, M. Marshall, S. Maurice, M. N. Puterbaugh and A. Widmer for access to unpublished data. This work was supported by a Fellowship from CONACyT to M. López-Villavicencio. The MENRT funded C. L. Collin.

Author information

Authors and Affiliations

  1. Laboratoire d'Ecologie Systématique et Evolution, CNRS UPRESA 8079, Université Paris-Sud XI, Bâtiment 360, 91405, Orsay Cedex, France

    Jacqui A. Shykoff, Sergios-Orestis Kolokotronis, Carine L. Collin & Manuela López-Villavicencio

Authors
  1. Jacqui A. Shykoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergios-Orestis Kolokotronis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carine L. Collin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manuela López-Villavicencio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jacqui A. Shykoff.

Appendix

Appendix

Summary

Table 3 shows a summary of the studies included in the metaanalysis.

Table 3. Summary of studies included in the metanalysis. Species are classified as to whether each flower contains a small fixed number of ovules (Few) or a large variable number (Many). NS No significant difference between females (F) and hermaphrodites (H), F≤H or F≥H both significant and non-significant differences found for different populations, F>H or F<H significant differences, * denotes results of supplemental hand pollination
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shykoff, J.A., Kolokotronis, SO., Collin, C.L. et al. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135, 1–9 (2003). https://doi.org/10.1007/s00442-002-1133-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-002-1133-z

Keywords

Search

Navigation