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Heritability and variance components of seed size in wild species: influences of breeding design and the number of genotypes tested

Abstract

Seed size affects individual fitness in wild plant populations, but its ability to evolve may be limited by low narrow-sense heritability (h2). h2 is estimated as the proportion of total phenotypic variance (σ2P) attributable to additive genetic variance (σ2A), so low values of h2 may be due to low σ2A (potentially eroded by natural selection) or to high values of the other factors that contribute to σ2P, such as extranuclear maternal effects (m2) and environmental variance effects (e2). Here, we reviewed the published literature and performed a meta-analysis to determine whether h2 of seed size is routinely low in wild populations and, if so, which components of σ2P contribute most strongly to total phenotypic variance. We analyzed available estimates of narrow-sense heritability (h2) of seed size, as well as the variance components contributing to these parameters. Maternal and environmental components of σ2P were significantly greater than σ2A, dominance, paternal, and epistatic components. These results suggest that low h2 of seed size in wild populations (the mean value observed in this study was 0.13) is due to both high values of maternally derived and environmental (residual) σ2, and low values of σ2A in seed size. The type of breeding design used to estimate h2 and m2 also influenced their values, with studies using diallel designs generating lower variance ratios than nested and other designs. e2 was not influenced by breeding design. For some breeding designs, the number of genotypes included in a study also influenced the resulting h2 and e2 estimates, but not m2. Our data support the view that a diallel design is better suited than the alternatives for the accurate estimation of σ2A in seed size due to its factorial design and the inclusion of reciprocal crosses, which allows the independent estimation of both additive and non-additive components of variance.

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Fig. 1: Marginal means of the alternative variance ratios extracted from a generalized quasi-binomial mixed-effects model.
Fig. 2: Marginal means from three generalized quasi-binomial mixed-effects models which represent three variance ratios separately as response variables as a function of breeding design, the number of genotypes, and the interaction between breeding design and the number of genotypes.

Data availability

Database and R code are available at the Dryad data repository https://doi.org/10.25349/D9660G.

References

  • Andersson S (1992) Quantitative genetic variation in a population of Crepis tectorum subsp. pumila (Asteraceae). Biol J Linn Soc 44(4):381–393

    Article  Google Scholar 

  • Antonovics J, Schmitt J (1986) Paternal and maternal effects on propagule size in Anthoxanthum odoratum. Oecologia 69(2):277–282

    Article  PubMed  Google Scholar 

  • Biere A (1991) Parental effects in Lychnis flos-cuculi. I: seed size, germination and seedling performance in a controlled environment. J Evolut Biol 4(3):447–465

    Article  Google Scholar 

  • Bonfil C (1998) The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae). Am J Bot 85(1):79–87

    Article  CAS  PubMed  Google Scholar 

  • Byers DL, Platenkamp GAJ, Shaw RG (1997) Variation in seed characters in Nemophila menziesii: evidence of a genetic basis for maternal effect. Evolution 51(5):1445–1456

    PubMed  Google Scholar 

  • Caignard T, Delzon S, Bodénès C, Dencausse B, Kremer A (2018) Heritability and genetic architecture of reproduction-related traits in a temperate oak species. Tree Genet Genomes 15(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  • Cain ML, Kahn B, Silander Jr JA, Reynolds HL (1995) Genetic variability and tradeoffs among reproductive traits in white clover (Trifolium repens). Can J Bot 73(3):505–511

    Article  Google Scholar 

  • Castellanos MC, Medrano M, Herrera CM (2008) Subindividual variation and genetic versus environmental effects on seed traits in a European Aquilegia. Botany 86(10):1125–1132

    Article  Google Scholar 

  • Cideciyan MA, Malloch AJC (1982) Effects of Seed Size on the Germination, Growth and Competitive Ability of Rumex Crispus and Rumex Obtusifolius. J Ecol 70(1):227–232

    Article  Google Scholar 

  • Cockerham CC, Weir BS (1977) Quadratic analyses of reciprocal crosses. Biometrics 33(1):187–203

    Article  CAS  PubMed  Google Scholar 

  • Crnokrak P, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75(5):530–540

    Article  Google Scholar 

  • Dalling JW, Hubbell SP (2002) Seed size, growth rate and gap microsite conditions as determinants of recruitment success for pioneer species. J Ecol 90(3):557–568

    Article  Google Scholar 

  • Dickerson G (1947) Composition of hog carcasses as influenced by heritable differences in rate and economy of gain. Iowa Agric Exp Station Res Bull 354:489–524

    Google Scholar 

  • Falconer DS, MacKay TFC (1996) Introduction to Quantitative Genetics, 4th ed. edn. Prentice Hall, Harlow, UK

    Google Scholar 

  • Fox J, Weisberg S (2019) Vol. 3rd. Sage, Thousand Oaks, California

    Google Scholar 

  • Galloway LF, Etterson JR, McGlothlin JW (2009) Contribution of direct and maternal genetic effects to life-history evolution. N. Phytologist 183(3):826–838

    Article  Google Scholar 

  • Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42(3):441–454

    Article  PubMed  Google Scholar 

  • Goodnight CJ (1995) Epistasis and the increase in additive genetic variance: implications for phase 1 of Wright’s shifting-balance process. Evolution 49(3):502–511

    PubMed  Google Scholar 

  • Gottlieb LD (1977) Phenotypic Variation in Stephanomeria exigua ssp. Coronaria (Compositae) and Its Recent Derivative Species “Malheurensis”. Am J Bot 64(7):873–880

    Article  Google Scholar 

  • Gustafsson L (1986) Lifetime reproductive success and heritability: empirical support for Fisher’s fundamental theorem. Am Naturalist 128(5):761–764

    Article  Google Scholar 

  • Hallauer AR, Carena MJ, Filho JBM (2010) Quantitative Genetics in Maize Breeding. Springer, New York

    Google Scholar 

  • Halpern SL (2005) Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses. Am J Bot 92(2):205–213

    Article  PubMed  Google Scholar 

  • Hill J, Becker HC, Tigerstedt PM (2012) Quantitative and Ecological Aspects of Plant Breeding. Springer, Netherlands

    Google Scholar 

  • Larios E, Venable DL (2015) Maternal adjustment of offspring provisioning and the consequences for dispersal. Ecology 96(10):2771–2780

    Article  PubMed  Google Scholar 

  • Larios E, Venable DL (2018) Selection for seed size: The unexpected effects of water availability and density. Funct Ecol 32(0):2216–2224

    Article  Google Scholar 

  • Lipow SR, Wyatt R (1999) Diallel crosses reveal patterns of variation in fruit-set, seed mass, and seed number in Asclepias incarnata. Heredity 83(3):310–318

    Article  PubMed  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer, Sunderland, MA, USA

    Google Scholar 

  • Madden LV, Piepho H-P, Paul PA (2016) Stat Models Methods Netw Meta-Anal Phytopathol® 106(8):792–806

    CAS  Google Scholar 

  • Mammen E, van de Geer S (1997) Penalized quasi-likelihood estimation in partial linear models. Ann Stat 25(3):1014–1035. 1022

    Article  Google Scholar 

  • Mazer SJ (1987) Parental effects on seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection. Evolution 41(2):355–371

    PubMed  Google Scholar 

  • Mazer SJ, Wolfe LM (1992) Planting Density Influences the Expression of Genetic Variation in Seed Mass in Wild Radish (Raphanus sativus L.: Brassicaceae). Am J Bot 79(10):1185–1193

    Article  PubMed  Google Scholar 

  • Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83(2):103–109

    Article  PubMed  Google Scholar 

  • Merilä J, Sheldon BC (2000) Lifetime Reproductive Success and Heritability in Nature. Am Naturalist 155(3):301–310

    Article  Google Scholar 

  • Mitchell-Olds T (1986) Quantitative genetics of survival and growth in Impatiens capensis. Evolution 40(1):107–116

    Article  PubMed  Google Scholar 

  • Mojonnier L (1998) Natural Selection on Two Seed Size Traits in the Common Morning Glory Ipomoea purpurea (Convolvulaceae): Patterns and Evolutionary Consequences. Am Naturalist 152(2):188–203

    Article  CAS  Google Scholar 

  • Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92(3):372–383

    Article  Google Scholar 

  • Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59(2):181–197

    Article  PubMed  Google Scholar 

  • Platenkamp GAJ, Shaw RG (1993) Environmental and Genetic Maternal Effects on Seed Characters in Nemophila menziesii. Evolution 47(2):540–555

    Article  PubMed  Google Scholar 

  • Rice KJ, Mack RN (1991) Ecological genetics of Bromus tectorum. Oecologia 88(1):77–83

    Article  PubMed  Google Scholar 

  • Ripley B, Venables B, Hornik K, Gebhardt A, Firth D (2013). MASS: Support Functions and Datasets for Venables and Ripley’s MASS. Modern Appl Stat S.

  • Roach DA, Wulff RD (1987) Maternal efects in plants. Annu Rev Ecol Syst 18(1):209–235

    Article  Google Scholar 

  • Schielzeth H, Dingemanse NJ, Nakagawa S, Westneat DF, Allegue H, Teplitsky C et al. (2020) Robustness of linear mixed-effects models to violations of distributional assumptions. Methods Ecol Evol 11(9):1141–1152

    Article  Google Scholar 

  • Searle SR, Speed FM, Milliken GA (1980) Population Marginal Means in the Linear Model: An Alternative to Least Squares Means. Am Stat 34(4):216–221

    Google Scholar 

  • Seiwa K, Kikuzawa K (1996) Importance of seed size for the establishment of seedlings of five deciduous broad-leaved tree species. Vegetatio 123(1):51–64

    Article  Google Scholar 

  • Shaw RG, Waser NM (1994) Quantitative Genetic Interpretations of Postpollination Reproductive Traits in Plants. Am Naturalist 143(4):617–635

    Article  Google Scholar 

  • Stanton ML (1984) Seed Variation in Wild Radish: Effect of Seed Size on Components of Seedling and Adult Fitness. Ecology 65(4):1105–1112

    Article  Google Scholar 

  • Thiede DA (1998) Maternal inheritance and its effect on adaptive evolution: a quantitative genetic analysis of maternal effects in a natural plant population. Evolution 52(4):998–1015

    Article  PubMed  Google Scholar 

  • Tucić B, Avramov S (1996) Maternal effects on early juvenile traits in Iris pumila (Iridaceae). Plant Syst Evol 201(1):179–197

    Article  Google Scholar 

  • Volis S (2007) Correlated patterns of variation in phenology and seed production in populations of two annual grasses along an aridity gradient. Evolut Ecol 21(3):381–393

    Article  Google Scholar 

  • Weber A, Kolb A (2014) Differences in heritable trait variation among populations of varying size in the perennial herb Phyteuma spicatum. Conserv Genet 15(6):1329–1337

    Article  Google Scholar 

  • Winn AA (1988) Ecological and evolutionary consequences of seed size in Prunella vulgaris. Ecology 69(5):1537–1544

    Article  Google Scholar 

  • Wolff K (1988) Genetic analysis of ecological relevant morphological variability in Plantago lanceolata L. Theor Appl Genet 75(5):772–778

    Article  Google Scholar 

  • Wulff RD (1986) Seed Size Variation in Desmodium Paniculatum: II. Effects on Seedling Growth and Physiological Performance. J Ecol 74(1):99–114

    Article  Google Scholar 

  • Zas R, Sampedro L (2015) Heritability of seed weight in Maritime pine, a relevant trait in the transmission of environmental maternal effects. Heredity 114(1):116–124

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank two anonymous reviewers who made insightful comments on the manuscript that helped improve the analysis and the results. Authors would also like to thank the UCMexus grant program for financial support for EL while he was in residence as a postdoctoral associate in the Department of Ecology, Evolution, and Marine Biology at UCSB. SJM is very grateful to the Yale Institute of Biospheric Studies, which provided sabbatical support during 2019-2020, when much of this work was conducted.

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EL and SJM designed the study and proposed hypotheses. EL extracted all values from the published literature and drafted the first version of the manuscript. EL and TRP performed statistical analyses. All authors contributed with the final version of the manuscript.

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Correspondence to Eugenio Larios.

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Larios, E., Ramirez-Parada, T.H. & Mazer, S.J. Heritability and variance components of seed size in wild species: influences of breeding design and the number of genotypes tested. Heredity 130, 251–258 (2023). https://doi.org/10.1038/s41437-023-00597-7

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