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Heritability and genetic architecture of reproduction-related traits in a temperate oak species

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Abstract

Reproduction, one of the main components of plant fitness, is highly variable in response to environmental cues, but little is known about the genetic determinism underlying reproduction-related traits in forest tree species. There is therefore an urgent need to characterize the genetic architecture of those traits if we are to predict the evolutionary trajectories of forest populations facing rapidly changing environment and mitigate their impacts. Using a full-sib family of pedunculate oak (Quercus robur), we investigated the within population variability of seed production and mean seed mass during four consecutive years. Reproductive traits were highly variable between trees and between years. The high narrow sense heritability and evolvability estimated underline the important genetic effect on the variability in seed production and mean seed mass. Despite a large variability over years, reproductive traits show significant genetic correlation between years. Furthermore, for the first time in forest tree species, quantitative trait loci (QTLs) associated with seed production and mean mass of a seed have been identified. While it is commonly assumed and observed that fitness traits have low narrow sense heritabilities, our findings show that reproduction-related traits may undergo evolutionary changes under selective pressure and may be determinant for tree adaptation.

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References

  • Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations: climate change outcomes for tree populations. Evol Appl 1:95–111

    Article  Google Scholar 

  • Alberto F, Bouffier L, Louvet JM, Delzon S, Kremer A (2011) Adaptive responses for seed and leaf phenology in natural populations of sessile oak along altitudinal gradients. J Evol Biol 24(7):1442–1454

    Article  CAS  Google Scholar 

  • Alonso-Blanco C, Vries HB, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci 96:4710–4717

    Article  CAS  Google Scholar 

  • Anderson JT (2016) Plant fitness in a rapidly changing world. New Phytol 210:81–87

    Article  Google Scholar 

  • Baliuckas V, Pliūra A, Eriksson G (2004) Forest tree breeding strategies in Nordic and Baltic countries and the possible implications on Lithuanian tree breeding strategy. Balt For 10(1):95–103

  • Barzdajn W (2008) Comparison of provenance, family and individual heritability of growth traits in pedunculate oak (Quercus robur L.) in the family-provenance trial in the Milicz Forest district. Sylwan 144(12):57–67 (in Polish)

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S et al (2014) lme4: linear mixed-effects models using Eigen and S4. R Package Version 1(7):1–23

    Google Scholar 

  • Beavis WD (1998) QTL analyses: power, precision, and accuracy. Molecular dissection of complex traits. CRC Press, New York, pp 145–162

  • Bilir N, Prescher F, Ayan S, Lindgren D (2006) Growth characters and number of strobili in clonal seed orchards of Pinus sylvestris. Euphytica 152:1–9

    Article  Google Scholar 

  • Bodénès C, Chancerel E, Ehrenmann F, Kremer A, Plomion C (2016) High-density linkage mapping and distribution of segregation distortion regions in the oak genome. DNA Res 23:115–124

    Article  Google Scholar 

  • Bogdan S, Katicic-Trupcevic, Kajab D (2004) Genetic variation in growth traits in a Quercus robur L. open-pollinated progeny test of the Slavonian provenance. Silvae Genet 53:198–201

  • Bogdan S, Ivankovic M, Temunovic M, Moric M, Franjic J, Bogdan IK (2017) Adaptive genetic variability and differentiation of Croatian and Austrian Quercus robur L. populations at a drought prone field trial. Annals of. For Res 60:33–46

    Google Scholar 

  • Bogdziewicz M, Fernández-Martínez M, Bonal R, Belmonte J, Espelta JM (2017) The Moran effect and environmental vetoes: phenological synchrony and drought drive seed production in a Mediterranean oak. Proc R Soc B 284:20171784

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  Google Scholar 

  • Bonal R, Muñoz A, Díaz M (2007) Satiation of predispersal seed predators: the importance of considering both plant and seed levels. Evol Ecol 21:367–380

    Article  Google Scholar 

  • Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/QTL: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  Google Scholar 

  • Buonaccorsi JP, Elkinton J, Koenig W, Duncan RP, Kelly D, Sork V (2003) Measuring mast seeding behavior: relationships among population variation, individual variation and synchrony. J Theor Biol 224:107–114

    Article  Google Scholar 

  • Caignard T, Kremer A, Firmat C, Nicolas M, Venner S, Delzon S (2017) Increasing spring temperatures favor oak seed production in temperate areas. Sci Rep 7:8555

    Article  Google Scholar 

  • Camarero JJ, Albuixech J, López-Lozano R, Casterad MA, Montserrat-Martí G (2010) An increase in canopy cover leads to masting in Quercus ilex. Trees 24:909–918

    Article  Google Scholar 

  • Cornelius J (1994) Heritabilities and additive genetic coefficients of variation in forest trees. Can J For Res 24:372–379

    Article  Google Scholar 

  • Derory J, Scotti-Saintagne C, Bertocchi E, Dantec LL, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodénès C, Alberto F, Kremer A (2010) Contrasting relationships between the diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity 104:438–448

    Article  CAS  Google Scholar 

  • Dirlewanger E, Quero-García J, Dantec LL, Lambert P, Ruiz D, Dondini L, Illa E, Quilot-Turion B, Audergon J-M, Tartarini S, Letourmy P, Arús P (2012) Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity 109:280

    Article  CAS  Google Scholar 

  • Doligez A, Bouquet A, Danglot Y, Lahogue F, Riaz S, Meredith C, Edwards K, This P (2002) Genetic mapping of grapevine (Vitis vinifera) applied to the detection of QTLs for seedlessness and berry weight. Theor Appl Genet 105:780–795

    Article  CAS  Google Scholar 

  • Drobyshev I, Övergaard R, Saygin I, Niklasson M, Hickler T, Karlsson M, Sykes MT (2010) Masting behaviour and dendrochronology of European beech (Fagus sylvatica L.) in southern Sweden. For Ecol Manag 259:2160–2171

    Article  Google Scholar 

  • El-Kassaby YA, Barclay HJ (1992) Cost of reproduction in Douglas-fir. Can J Bot 70:1429–1432

    Article  Google Scholar 

  • Firmat C, Delzon S, Louvet JM, Parmentier J, Kremer A (2017) Evolutionary dynamics of the leaf phenological cycle in an oak metapopulation along an elevation gradient. J Evol Biol 30:2116–2131

    Article  CAS  Google Scholar 

  • Gómez JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:71–80

    Article  Google Scholar 

  • Guitton B, Kelner J-J, Velasco R, Gardiner SE, Chagné D, Costes E (2011) Genetic control of biennial bearing in apple. J Exp Bot 63:131–149

    Article  Google Scholar 

  • Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324

    Article  CAS  Google Scholar 

  • Hall D, Hallingbäck HR, Wu HX (2016) Estimation of number and size of QTL effects in forest tree traits. Tree Genet Genomes 12:110

    Article  Google Scholar 

  • Han Q, Kabeya D, Iio A, Kakubari Y (2008) Masting in Fagus crenata and its influence on the nitrogen content and dry mass of winter buds. Tree Physiol 28:1269–1276

    Article  Google Scholar 

  • Hansen TF, Pélabon C, Houle D (2011) Heritability is not Evolvability. Evol Biol 38:258–277

    Article  Google Scholar 

  • Haymes KL, Fox GA (2012) Variation among individuals in cone production in Pinus palustris (Pinaceae). Am J Bot 99:640–645

    Article  Google Scholar 

  • Hoffmann AA, Merilä J, Kristensen TN (2016) Heritability and evolvability of fitness and nonfitness traits: lessons from livestock. Evolution 70:1770–1779

    Article  Google Scholar 

  • Houel C, Chatbanyong R, Doligez A, Rienth M, Foria S, Luchaire N, Roux C, Adivèze A, Lopez G, Farnos M, Pellegrino A, This P, Romieu C, Torregrosa L (2015) Identification of stable QTLs for vegetative and reproductive traits in the microvine (Vitis vinifera L.) using the 18 K Infinium chip. BMC Plant Biol 15:205

    Article  Google Scholar 

  • Howe H, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13(1):201–228

    Article  Google Scholar 

  • Ishihara MI, Kikuzawa K (2009) Annual and spatial variation in shoot demography associated with masting in Betula grossa: comparison between mature trees and saplings. Ann Bot 104:1195–1205

    Article  Google Scholar 

  • Jensen JS, Wellendorf H, Jager K, De Vries SMG, Jensen V (1997) Analysis of a 17-year old Dutch open-pollinated progeny trial with Quercus robur (L.). For Genet 4(3):139–147

    Google Scholar 

  • Jermstad KD, Bassoni DL, Jech KS, Wheeler NC, Neale DB (2001) Mapping of quantitative trait loci controlling adaptive traits in coastal Douglas-fir. I. Timing of vegetative bud flush. Theor Appl Genet 102:1142–1151

    Article  CAS  Google Scholar 

  • Kadri A, Julier B, Laouar M, Ben C, Badri M, Chedded J, Mouhouche B, Gentzbittel L, Abdelguerfi A (2017) Genetic determinism of reproductive fitness traits under drought stress in the model legume Medicago truncatula. Acta Physiol Plant 39:227

    Article  Google Scholar 

  • Kang K-S, Bila AD, Harju AM, Lindgren D (2003) Estimation of fertility variation in forest tree populations. Forestry 76:329–344

    Article  Google Scholar 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447

    Article  Google Scholar 

  • Knops JM, Koenig WD, Carmen WJ (2007) Negative correlation does not imply a tradeoff between growth and reproduction in California oaks. Proc Natl Acad Sci 104:16982–16985

    Article  CAS  Google Scholar 

  • Koenig WD, Knops JMH (1998) Scale of mast-seeding and tree-ring growth. Nature 396:225–226

    Article  CAS  Google Scholar 

  • Koenig WD, Mumme RL, Carmen WJ, Stanback MT (1994) Acorn production by oaks in central coastal California: variation within and among years. Ecology 75:99–109

    Article  Google Scholar 

  • Koenig WD, Knops JM, Carmen WJ, Stanback MT, Mumme RL (1996) Acorn production by oaks in central coastal California: influence of weather at three levels. Can J For Res 26:1677–1683

    Article  Google Scholar 

  • Koenig WD, Knops JMH, Dickinson JL, Zuckerberg B (2009) Latitudinal decrease in acorn size in bur oak ( Quercus macrocarpa ) is due to environmental constraints, not avian dispersal. Botany 87:349–356

    Article  Google Scholar 

  • Kroon J, Wennström U, Prescher F, Lindgren D, Mullin TJ (2009) Estimation of clonal variation in seed cone production over time in a scots pine (Pinus sylvestris L.) seed orchard. Silvae Genet 58(1–6):53–62

  • Lesur I, Alexandre H, Boury C, Chancerel E, Plomion C, Kremer A (2018) Development of target sequence capture and estimation of genomic relatedness in a mixed oak stand. Front Plant Sci 9:996

  • Lopez-Toledo L, Heredia-Hernández M, Castellanos-Acuña D, Blanco-García A, Saénz-Romero C (2017) Reproductive investment of Pinus pseudostrobus along an altitudinal gradient in Western Mexico: implications of climate change. New For 48(6):867–881

    Article  Google Scholar 

  • Manichaikul A, Dupuis J, Sen Ś, Broman KW (2006) Poor performance of bootstrap confidence intervals for the location of a quantitative trait locus. Genetics 174:481–489

    Article  Google Scholar 

  • Manichaikul A, Moon JY, Sen Ś, Yandell BS, Broman KW (2009) A model selection approach for the identification of quantitative trait loci in experimental crosses, allowing epistasis. Genetics 181:1077–1086

    Article  CAS  Google Scholar 

  • Mather RA, Kanowski PJ, Savill PS (1993) Genetic determinism of vessel area in oak (Quercus robur L. and Q.petraea Liebl): a characteristic related to the occurrence of stem sakes. Ann For Sci 50(Suppl1):395s–398s

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Mitchell-Olds T (1996) Genetic constraints on life-history evolution: quantitative-trait loci influencing growth and flowering in Arabidopsis Thaliana. Evolution 50:140–145

    Article  Google Scholar 

  • Monks A, Kelly D (2006) Testing the resource-matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae). Austral Ecol 31:366–375

    Article  Google Scholar 

  • Mutke S, Gordo J, Gil L (2005) Cone yield characterization of a stone pine (Pinus pinea L.) clone bank. Silvae Genet 54(1–6):189–197

  • Nepveu G (1984a) Genotypic determination of the anatomical structure of wood in Quercus robur. Silvae Genet 33(2–3):91–95

  • Nepveu G (1984b) Hereditary control of density and retractability of wood from 3 oak species (Quercus petraea, Quercus robur and Quercus rubra). Silvae Genet 33(4–5):110–115

  • Nikkanen T, Ruotsalainen S (2000) Variation in flowering abundance and its impact on the genetic diversity of the seed crop in a Norway spruce seed orchard. Silva Fenn 34(3):205–222

    Article  Google Scholar 

  • Pearse IS, Koenig WD, Kelly D (2016) Mechanisms of mast seeding: resources, weather, cues, and selection. New Phytol 212(3):546–562

    Article  CAS  Google Scholar 

  • Pelgas B, Bousquet J, Meirmans PG, Ritland K, Isabel N (2011) QTL mapping in white spruce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genomics 12:145

    Article  Google Scholar 

  • Pérez-Ramos IM, Ourcival JM, Limousin JM, Rambal S (2010) Mast seeding under increasing drought: results from a long-term data set and from a rainfall exclusion experiment. Ecology 91:3057–3068

    Article  Google Scholar 

  • Pérez-Ramos IM, Aponte C, García LV, Padilla-Díaz CM, Marañón T (2014) Why is seed production so variable among individuals? A ten-year study with oaks reveals the importance of soil environment. PLoS One 9:e115371

    Article  Google Scholar 

  • Plomion C, Aury JM, Amselem J, Alaeitabar T, Barbe V, Belser C, Berges H, Bodénès C, Boudet N, Boury C, Canaguier A, Couloux A, Da Silva C, Duplessis S, Ehrenmann F, Estrada-Mairey B, Fouteau S, Francillonne N, Gaspin C, Guichard C, Klopp C, Labadie K, Lalanne C, Le Clainche I, Leplé JC, Le Provost G, Leroy T, Lesur I, Martin F, Mercier J, Michotey C, Murat F, Salin F, Steinbach D, Faivre-Rampant P, Wincker P, Salse J, Quesneville H, Kremer A (2016) Decoding the oak genome: public release of sequence data, assembly, annotation and publication strategies. Mol Ecol Resour 16:254–265

    Article  CAS  Google Scholar 

  • Price T, Schluter D (1991) On the low heritability of life-history traits. Evolution 45:853–861

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Romeu JF, Monforte AJ, Sánchez G, Granell A, García-Brunton J, Badenes ML, Ríos G (2014) Quantitative trait loci affecting reproductive phenology in peach. BMC Plant Biol 14:52

    Article  Google Scholar 

  • Sadok IB, Celton J-M, Essalouh L, Aabidine AZE, Garcia G, Martinez S, Grati-Kamoun N, Rebai A, Costes E, Khadari B (2013) QTL mapping of flowering and fruiting traits in olive. PLoS One 8:e62831

    Article  Google Scholar 

  • Saintagne C, Bodénès C, Barreneche T, Pot D, Plomion C, Kremer A (2004) Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 92:20–30

    Article  CAS  Google Scholar 

  • Sanchez-Humanes B, Espelta JM (2011) Increased drought reduces acorn production in Quercus ilex coppices: thinning mitigates this effect but only in the short term. Forestry 84:73–82

    Article  Google Scholar 

  • Santos del Blanco L, Zas R, Notivol Paíno E, Chambel MR, Majada J, Climent J (2010) Variation of early reproductive allocation in multi-site genetic trials of maritime pine and Aleppo pine. Variación en asignación reproductiva temprana en ensayos multi-localidad de pino carrasco y pino negra. For Syst 19:381–392

    Google Scholar 

  • Santos-del-Blanco L, Climent J, González-Martínez SC, Pannell JR (2012) Genetic differentiation for size at first reproduction through male versus female functions in the widespread Mediterranean tree Pinus pinaster. Ann Bot 110:1449–1460

    Article  CAS  Google Scholar 

  • Savill PS, Kanowski PJ, Gourlay ID, Jarvis AR (1993) Genetic and intra tree variation in the number of sapwood rings in Quercus robur and Q. petraea. Silvae Genet 42:371–375

    Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353

    Article  Google Scholar 

  • Scotti-Saintagne C, Bodénès C, Barreneche T, Bertocchi E, Plomion C, Kremer A (2004) Detection of quantitative trait loci controlling bud burst and height growth in Quercus robur L. Theor Appl Genet 109:1648–1659

    Article  CAS  Google Scholar 

  • Shalom L, Samuels S, Zur N, Shlizerman L, Zemach H, Weissberg M, Ophir R, Blumwald E, Sadka A (2012) Alternate bearing in Citrus: changes in the expression of flowering control genes and in global gene expression in ON- versus OFF-crop trees. PLoS One 7:e46930

    Article  CAS  Google Scholar 

  • Silvertown J, Dodd M (1999) The Demographic Cost of Reproduction and Its Consequences in Balsam Fir ( Abies balsamea ). Am Nat 154:321–332

    Article  Google Scholar 

  • Sirois L (2000) Spatiotemporal variation in black spruce cone and seed crops along a boreal forest - tree line transect. Can J For Res 30:900–909

    Article  Google Scholar 

  • Sıvacıoglu A, Ayan S, Çelik D (2009) Clonal variation in growth, flowering and cone production in a seed orchard of scots pine (Pinus sylvestris L.) in Turkey. Afr J Biotechnol 8(17):4084–4093

  • Sousa WP, Kennedy PG, Mitchell BJ (2003) Propagule size and predispersal damage by insects affect establishment and early growth of mangrove seedlings. Oecologia 135:564–575

    Article  Google Scholar 

  • Traveset A, Heleno R, Nogales M (2014) The ecology of seed dispersal. Seeds: the ecology of regeneration in plant. communities 3:62–93

    Google Scholar 

  • Tsubomura M, Fukatsu E, Nakada R, Fukuda Y (2012) Inheritance of male flower production in Cryptomeria japonica (sugi) estimated from analysis of a diallel mating test. Ann For Sci 69:867–875

    Article  Google Scholar 

  • Ujino-Ihara T, Iwata H, Taguchi Y, Tsumura Y (2012) Identification of QTLs associated with male strobilus abundance in Cryptomeria japonica. Tree Genet Genomes 8:1319–1329

    Article  Google Scholar 

  • Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philosophical transactions of the Royal Society of London B. Biol Sci 365(1542):989–997

    Article  Google Scholar 

  • Vinkhuyzen AA, Wray NR, Yang J, Goddard ME, Visscher PM (2013) Estimation and partition of heritability in human populations using whole-genome analysis methods. Annu Rev Genet 47(1):75–95

    Article  CAS  Google Scholar 

  • Visscher PM, Goddard ME (2014) A general unified framework to assess the sampling variance of heritability estimates using pedigree or marker-based relationships. Genetics 199(1):223–232

    Article  Google Scholar 

  • Walters MB, Reich PB (2000) Seed size, nitrogen supply, and growth rate affect tree seedling survival in deep shade. Ecology 81:1887–1901

    Article  Google Scholar 

  • White TL, Adams WT, Neale DB (Eds.) (2007) Forest genetics. Cabi

  • Wu J, Li L-T, Li M, Khan MA, Li X-G, Chen H, Yin H, Zhang S-L (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the experimental units of Bourran (UE 0393 INRA, Domaine de la Tour de Rance 47320 Bourran, France) and Toulenne (UE 0393 INRA, Domaine des Jarres 33210 Toulenne, France) for technical support. We thank Jérôme Bartholomé for his assistance in the QTL analysis.

Data archiving statement

http://mapedigree.pierroton.inra.fr/qmap/

Funding

This research was supported by the European Research Council through the Advanced Grant Project TREEPEACE (#FP7-339728). TC received a PhD grant from TREEPEACE and the Initiative of Excellence program (IdEX-03-02) of Bordeaux University. BIOGECO is supported by a grant overseen by the French National Research Agency (ANR) as part of the “Investissements d’Avenir” through the Cluster of Excellence COTE (ANR-10-LABEX45).

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T.C. and A.K. conceived the idea for this work; T.C. and B.D. assembled the dataset; T.C and C.B. analyzed the data; T.C. and A.K. wrote the manuscript; and C.B. and S.D. revised the manuscript.

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Correspondence to Thomas Caignard.

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Communicated by P. Ingvarsson

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Caignard, T., Delzon, S., Bodénès, C. et al. Heritability and genetic architecture of reproduction-related traits in a temperate oak species. Tree Genetics & Genomes 15, 1 (2019). https://doi.org/10.1007/s11295-018-1309-2

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