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Inbreeding depression from selfing and mating between relatives in the Neotropical tree Cariniana legalis Mart. Kuntze

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Abstract

Selfing or mating between related individuals in self-compatible hermaphroditic tree species may lead to inbreeding depression (ID) due to homozygosis in recessive, identical by descent alleles. In general, studies of ID in tree species have been based on comparisons of selfed individuals (produced by controlled pollination) with outcrossed individuals for quantitative traits in progeny tests. However, this approach requires a long time to quantify the extent of ID. Thus, we used an approach based on genetic markers to estimate coancestry coefficients between assigned parents from paternity analysis in two populations of the Neotropical tree Cariniana legalis. Using this method, we were able to determine which seedlings in a nursery trial originated from; (i) outcrossing between un-related trees, (ii) mating between related trees and (iii) selfing. We detected a low selfing rate (<10 %), but a substantial quantity of seedlings from mating between related parents (minimum of 35.7 %). In general, the outcrossed seedlings from unrelated parents exhibited significantly greater genetic diversity than those resulting from selfing and mating among relatives. The extent of ID varied among traits and populations. Outcrossed seedlings originating from unrelated trees generally showed greater survival than seedlings originating from selfing and related parents. Inbreeding depression was greater in the selfed seedlings than in those from mating among related parents. The results are discussed in terms of implications for genetic conservation, breeding and environmental restoration using the species.

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References

  • Bittencourt JM, Sebbenn AM (2007) Patterns of pollen and seed dispersal in a small fragmented population of a wind pollinated Araucaria angustifolia in southern Brazil. Heredity 99:580–591

    Article  CAS  PubMed  Google Scholar 

  • Blouin MS, Parsons M, Lacaille V, Lotz S (1996) Use of microsatellite loci to classify individuals by relatedness. Mol Ecol 5:393–401

    Article  CAS  PubMed  Google Scholar 

  • Byers DL, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513

    Article  Google Scholar 

  • Carvalho PER (2003) Espécies arbóreas brasileiras. Embrapa Informação Tecnológica, Brasília

    Google Scholar 

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

    Article  Google Scholar 

  • Chaves LJ, Vencovsky R, Silva RSM, Telles MPC, Zucchi MI, Coelho ASG (2011) Estimating inbreeding depression in natural plant populations using quantitative and molecular data. Conserv Genet 12:569–576

    Article  Google Scholar 

  • Degen B, Sebbenn AM (2014) Genetics and tropical forests. In: Pancel L, Kölh M (eds) Tropical forestry handbook, 2nd edn. Springer, Berlin, pp 885–920

    Google Scholar 

  • Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biol 1:20–33

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Falconer DS, Mackay TFC (1997) Introduction to quantitative genetics. Longman Group Ltd, Harlow

    Google Scholar 

  • Goudet J (1995) Fstat (Version 2.9.3.2.): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Griffin AR, Cotterill PP (1988) Genetic variation in growth of outcrossed, selfed and open-pollinated progenies of Eucalyptus regnans end some implications for breeding strategy. Silvae Genet 37:124–131

    Google Scholar 

  • Hardy O, Vekemans X (2002) SPAGeDI: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hufford KM, Hamrick JL (2003) Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57:518–526

    Article  PubMed  Google Scholar 

  • Ismail SA, Ghazoul J, Ravikanth G, Uma Shaanker R, Kushalappa CG, Kettle CJ (2012) Does long-distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro-forest landscape. Mol Ecol 21:5484–5496

    Article  CAS  PubMed  Google Scholar 

  • Ismail SA, Ghazoul J, Ravikanth G, Uma Shaanker R, Kushalappa CG, Kettle CJ (2014) Fragmentation genetics of Vateria indica: implications for management of forest genetic resources of an endemic dipterocarp. Conserv Genet 15:533–545

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kärkkäinen K, Savolainen O (1996) 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

    Article  Google Scholar 

  • Koelewijn HP, Koski V, Savolainen O (1999) Magnitude and timing of inbreeding depression in Scots Pine (Pinus sylvestris L.). Evolution 53:758–768

    Article  Google Scholar 

  • Lindgren D, Luigi DG, Jefferson PA (1997) Status number for measuring genetic diversity. Forest Genet 4:69–76

    Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273

    Article  CAS  PubMed  Google Scholar 

  • Manoel RO, Alves PF, Dourado CL, Gaino APSC, Freitas MLM, Moraes MLT, Sebbenn AM (2012) Contemporary pollen flow, mating patterns and effective population size inferred from paternity analysis in a small fragmented population of the Neotropical tree Copaifera langsdorffii Desf. (Leguminosae-Caesalpinioideae). Conserv Genet 13:613–623

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • Meagher TR, Thompson E (1987) Analysis of parentage for naturally established seedlings of Chamaelirium luteum (Liliaceae). Ecology 68:803–812

    Article  Google Scholar 

  • Naito Y, Konuma A, Iwata YS, Seiwa K, Okuda T, Lee SL, Muhammad N, Tsumura Y (2005) Selfing and inbreeding depression in seeds and seedlings of Neobalanocarpus heimii (Dipterocarpaceae). J Plant Res 118:423–430

    Article  PubMed  Google Scholar 

  • Prance GT, Mori SA (1979) Lecythidaceae—part 1, flora neotropica monograph 21. NY Bot Gard, New York, pp 1–272

    Google Scholar 

  • Ritland K (1996) Inferring the genetic basis of inbreeding depression in plants. Genome 39:1–8

    Article  CAS  PubMed  Google Scholar 

  • Rymer PD, Sandiford M, Harris SA, Billingham MR, Boshier DH (2015) Remnant Pachira quinata pasture trees have greater opportunities to self and suffer reduced reproductive success due to inbreeding depression. Heredity 115:115–124

    Article  CAS  PubMed  Google Scholar 

  • SAS (1999) Institute Inc. SAS procedures guide. Version 8 (TSMO). SAS, Cary

  • Sebbenn AM, Kageyama PY, Siqueira ACMF, Zanatto ACS (2000) Sistema de cruzamento em populações de Cariniana legalis Mar. O. Ktze.: implicações para a conservação e o melhoramento genético. Sci For 58:24–40

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: principles and practices of statistics in biological research, 3rd edn. W.H. Freeman and Company, New York

    Google Scholar 

  • Sorensen FC (1997) Effects of sib mating and wind pollination on nursery seedling size, growth components, and phenology of Douglas-fir seed-orchard progenies. Can J For Res 27(4):557–566

    Article  Google Scholar 

  • Sorensen FC, Miles R (1982) Inbreeding depression in height, height growth and survival of Douglas-Fr, Ponderosa Pine, and Noble Fir to 10 years of age. For Sci 28:283–292

    Google Scholar 

  • Tambarussi EV, Sebbenn AM, Moreno MA, Ferraz EM, Kageyama PY, Vencovsky R (2013a) Microsatellite markers for Cariniana legalis (Lecythidaceae) and their transferability to Cariniana estrellensis. Appl Plant Sci 1:1200493

    Article  Google Scholar 

  • Tambarussi EV, Vencovsky R, Freitas MLM, Sebbenn AM (2013b) Mendelian inheritance, genetic linkage and genotypic disequilibrium at nine microsatellite loci of Cariniana legalis (Mart.) O. Kuntze. Genet Mol Res 12:5442–5457

    Article  CAS  PubMed  Google Scholar 

  • Tambarussi EV, Boshier DH, Vencovsky R, Freitas MLM, Di-Dio O-J, Ferraz EM, Moreno MA, Sebbenn AM (2015) Paternity analysis reveals significant isolation and near neighbour pollen dispersal in small Cariniana legalis Mart. Kuntze populations in the Brazilian Atlantic Forest. Ecol Evol 5:5588–5600

    Article  PubMed  PubMed Central  Google Scholar 

  • Winn AA, Elle E, Kalisz S, Cheptou PO, Eckert CG, Goodwillie C, Johnston MO, Moeller DA, Ree RH, Sargent RD, Vallejo-Marín M (2011) Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65:3339–3359

    Article  PubMed  Google Scholar 

  • Wu HX, Matheson AC, Spencer D (1998) Inbreeding in Pinus radiata. 1. The effect of inbreeding on growth, survival and variance. Theor Appl Genet 97:1256–1268

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP - 2010/10704-7) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - 470491/2010-8) for funding this project. Evandro V. Tambarussi was supported by a FAPESP PhD scholarship (grant 2010/12354-3). Alexandre M. Sebbenn, Miguel L.M. Freitas and Roland Vencovsky are supported by CNPq research fellowships. We thank Tiago Gabassi for help in the laboratory and Wladimir Correa and Dirceu de Souza for their help in collecting the plant samples. We also thank NPGLE for corrections to the English.

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Correspondence to Evandro Vagner Tambarussi.

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Tambarussi, E.V., Boshier, D., Vencovsky, R. et al. Inbreeding depression from selfing and mating between relatives in the Neotropical tree Cariniana legalis Mart. Kuntze. Conserv Genet 18, 225–234 (2017). https://doi.org/10.1007/s10592-016-0896-4

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