Skip to main content
Log in

Why do plants abort so many developing seeds: bad offspring or bad maternal genotypes?

  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

It has been suggested that abortion of ovules in perennials is caused partly by early acting genetic load (abortions due to ‘bad offspring’). However, it is still unclear what proportion of abortions of naturally pollinated seeds are due to early genetic load. Here we suggest that variation between maternal genotypes (abortions due to ‘bad maternal genotypes’) may be an even more important factor causing genetic abortions than early load, based on results from Scots pine. The early load is severe in Scots pine: in experimental self-pollinations on average 76% of the seeds were aborted. Comparison of naturally pollinated and experimentally cross-pollinated seeds showed that the abortion rate of naturally pollinated seeds was only slightly, and not statistically significantly, higher than that of experimentally cross-pollinated seeds (30% vs. 26.5%, respectively). Thus, although early load can be high under self-pollination in Scots pine, it does not account for a high share of abortions of naturally pollinated seeds. Instead, maternal genotype determined the seed abortion rate: in a separate experiment using an experimental population (clonal stand), 29% of the total variance in seed abortion was due to variation between maternal genotypes. We studied further whether ‘bad maternal genotypes’ could be explained by trade-offs between seed abortion and other fitness functions. Only one statistically significant genetic correlation was found, a positive association between cone production and successful seed development. Thus ‘bad maternal genotypes’ aborted a higher proportion of their seed and produced less cones than the ‘good maternal genotypes’.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ågren, J. (1988) Between-year variation in flowering and fruit set in frost-prone and frost-sheltered populations of dioecious Rubus chamaemoms. Oecologia 76, 175–183.

    Article  Google Scholar 

  • Andersson, S. (1993) The potential for selective seed maturation in Achillea ptarmica (Asteraceae). Oikos 66, 36–42.

    Google Scholar 

  • Bawa, K.S. and Webb, C.J. (1984) Flower, fruit and seed abortion in tropical forest trees: implications for the evolution of paternal and maternal reproductive patterns. Am. J. Bot. 71, 736–751.

    Article  Google Scholar 

  • Bishir, J. and Namkoong, G. (1987) Unsound seeds in conifers: estimation of numbers of lethal alleles and of magnitudes of effects associated with the maternal parent. Silvae Genetica 36, 180–185.

    Google Scholar 

  • Burbidge, A.H. and James, S.H. (1991) Postzygotic seed abortion in the genetic system of Stylidium (Angiospermae: Stylidaceae). J. Heredity 82, 319–328.

    Google Scholar 

  • Casper, B.B. (1984) On the evolution of embryo abortion in the herbaceous perennial Cryptantha (Boraginaceae). Evolution 38, 1337–1349.

    Article  Google Scholar 

  • Charlesworth, D. (1989) Evolution of low female fertility in plants: pollen limitation, resource allocation and genetic load. Trends Ecol. Evol. 4, 289–292.

    Article  Google Scholar 

  • Charlesworth, D. and Charlesworth, B. (1987a) The effect of investment in attractive structures on allocation to male and female functions in plants. Evolution 41, 948–968.

    Article  Google Scholar 

  • Charlesworth, D. and Charlesworth, B. (1987b) Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst. 18, 237–268.

    Article  Google Scholar 

  • Ehrlén, J. (1991) Why do plants produce surplus flowers? A reserve-ovary model. Am. Nat. 138, 918–933.

    Article  Google Scholar 

  • Falconer, D.S. (1989) Introduction to Quantitative Genetics. Longman, Essex, UK.

    Google Scholar 

  • Fu, Y.-B. and Ritland, K. (1994) Evidence for the partial dominance of viability genes contributing to inbreeding depression in Mimulus guttatus. Genetics 136, 323–331.

    PubMed  CAS  Google Scholar 

  • Griffin, A.R. and Lindgren, D. (1985) Effect of inbreeding on production of filled seed in Pinus radiata — experimental results and a model of gene action. Theor. Appl. Genet. 71, 334–343.

    Google Scholar 

  • Hedrick, P.W. (1987) Genetic load and the mating system in homosporous ferns. Evolution 41, 1282–1289.

    Article  Google Scholar 

  • Holtsford, T.P. (1985) Nonfruiting hermaphroditic flowers of Calochortus leichtlinii (Liliaceae): potential reproductive functions. Am. J. Bot. 72, 1687–1694.

    Article  Google Scholar 

  • Houle, D. (1992) Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204.

    PubMed  CAS  Google Scholar 

  • Johnsson, H. (1976) Contributions to the genetics of empty grains in the seed of Scots pine (Pinus sylvestris). Silvae Genet. 25, 10–15.

    Google Scholar 

  • Kärkkäinen, K. and Savolainen, O. (1993) The degree of early inbreeding depression determines the selfing rate at the seed stage: model and results from Pinus sylvestris (Scots pine). Heredity 71, 160–166.

    Google Scholar 

  • Kärkkäinen, K., Koski, V. and Savolainen, O. (1996) Geographical variation in the early inbreeding depression of Scots pine. Evolution 50, 111–119.

    Article  Google Scholar 

  • Kärkkäinen, K., Kuittinen, H., van Treuren, R., Vogl, C, Oikarinen, S. and Savolainen, O. (1999) Genetic basis of inbreeding depression in Arabis petraea. Evolution 53, 1354–1365.

    Article  Google Scholar 

  • Kempthorne, O. (1957) An Introduction to Genetic Statistics. The Iowa State University Press, Ames, IA.

    Google Scholar 

  • Klekowski, E.J. Jr. (1988a) Genetic load and its causes in long-lived plants. Trees 1988, 195–203.

    Google Scholar 

  • Klekowski, E.J. Jr. (1988b) Progressive cross-and self-sterility associated with aging in fern clones and perhaps other plants. Heredity 61, 247–253.

    Google Scholar 

  • Klekowski, E.J. Jr. and Godfrey, P.J. (1989) Ageing and mutation in plants. Nature 340, 389–391.

    Article  Google Scholar 

  • Koski, V. (1970) A study of pollen dispersal as a mechanism of gene flow in conifers. Commun. Inst. For. Fenn. 70.4, 1–78.

    Google Scholar 

  • Koski, V. (1971) Embryonic lethals of Picea abies and Pinus sylvestris. Commun. Inst. For. Fenn. 75.3, 1–30.

    Google Scholar 

  • Koski, V. and Muona, O. (1986) Probability of inbreeding in relation to clonal differences in male flowering and embryonic lethals. Proceedings of IUFRO conference on breeding theory, progeny testing and seed orchards, Williamsburgh, Virginia, 13–17 October, 1986, pp. 391–300.

  • Kozlowski, J. and Stearns, S.C. (1989) Hypotheses for the production of bet-hedging and selective abortion. Evolution 43, 1369–1377.

    Article  Google Scholar 

  • Krebs, S.L. and Hancock, J.F. (1991) Embryonic genetic load in the highbush blueberry, Vaccinium corymbosum (Ericaceae). Am. J. Bot. 78, 1427–1437.

    Article  Google Scholar 

  • Morgan, M. (1993) Fruit to flower ratios and trade-offs in size and number. Evol. Ecol. 7, 219–232.

    Article  Google Scholar 

  • Muona, O. and Harju, A. (1989) Effective population sizes, genetic variability, and mating system in natural stands and seed orchards of Pinus sylvestris. Silvae Genet. 38, 221–228.

    Google Scholar 

  • Obeso, J.R. (1993) Selective fruit and seed maturation in Asphodelus albus Miller (Liliaceae). Oecologia 93, 564–570.

    Article  Google Scholar 

  • Pellmyr, O. and Huth, C.J. (1994) Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372, 257–260.

    Article  CAS  Google Scholar 

  • Plym Forshell, C. (1974) Seed development after self-pollination and cross-pollination of Scots pine, Pinus sylvestris L. Studia Forestalia Suecica 118, 1–37.

    Google Scholar 

  • Roach, D.A. and Wulff, R.D. (1987) Maternal effects in plants. Ann. Rev. Ecol. Syst. 18, 209–235.

    Article  Google Scholar 

  • Sarvas, R. (1962) Investigation on the flowering and seed crop of Pinus sylvestris. Commun. Inst. For. Fenn. 53.4, 1–198.

    Google Scholar 

  • SAS Institute (1985) Users's Guide: Statistics. 1985 Edition. SAS Institute, Inc., Gary, NC.

    Google Scholar 

  • Savolainen, O. (1994) Genetic variation and fitness: conservation lessons from pines. In V. Loeschcke, J. Tomiuk and S.K. Jain (eds) Conservation Genetics, pp. 27–36. Birkhäuser, Basel.

    Google Scholar 

  • Savolainen, O. Kärkkäinen, K. and Kuittinen, H. (1992) Estimating numbers of embryonic lethals in conifers. Heredity 69, 308–314.

    Google Scholar 

  • Savolainen, O., Kärkkäinen, K., Harju, A., Nikkanen, T. and Rusanen, M. (1993) Fertility variation in Pinus sylvestris: a test of sexual allocation theory. Am. J. Bot. 80, 1016–1020.

    Article  Google Scholar 

  • Simmons, M.J. and Crow, J.F. (1977) Mutations affecting fitness in Drosophila populations. Ann. Rev. Genet. 11, 49–78.

    Article  PubMed  CAS  Google Scholar 

  • Smith, C.C., Hamrick, J.L. and Kramer, C.L. (1990) The advantage of mast years for wind pollination. Am. Nat. 136, 154–166.

    Article  Google Scholar 

  • Sorensen, F.C. (1969) Embryonic genetic load in coastal Douglas fir, Pseudotsuga menziesii var menziesii. Am. Nat. 103, 389–398.

    Article  Google Scholar 

  • Stephenson, A.G. (1981) Flower and fruit abortion: proximate causes and ultimate functions. Ann. Rev. Ecol. Syst. 12, 253–279.

    Article  Google Scholar 

  • Stern, K. (1972) Über die Ergebnisse einiger Versuche zur räumlichen und zeitlichen Verteilung des Pollens einzelner Kiefern. Z. Pflanzenzuchtung 67, 313–326.

    Google Scholar 

  • Sutherland, S. (1986) Patterns of fruit-set: what controls fruit-flower ratios in plants? Evolution 40, 117–128.

    Article  Google Scholar 

  • Wiens, D. (1984) Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64, 47–53.

    Article  Google Scholar 

  • Wiens, D., Calvin, C.L., Wilson, C.A. Davern, C.I., Frank, D. and Seavey, S.R. (1987) Reproductive success, spontaneous embryo abortion, and genetic load in flowering plants. Oecologia 71, 501–509.

    Article  Google Scholar 

  • Willis, J.H. (1993) Effects of different levels of inbreeding on fitness components in Mimulus guttatus. Evolution 47, 864–876.

    Article  Google Scholar 

  • Willson, M.F. and Rathcke, B.J. (1974) Adaptive design of the floral display in Asclepias syriaca L. Am. Midl Nat. 92, 47–57.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kärkkäinen, K., Savolainen, O. & Koski, V. Why do plants abort so many developing seeds: bad offspring or bad maternal genotypes?. Evolutionary Ecology 13, 305–317 (1999). https://doi.org/10.1023/A:1006746900736

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006746900736

Navigation