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All But Sleeping? Consequences of Soil Seed Banks on Neutral and Selective Diversity in Plant Species

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Abstract

An axiom of modern evolutionary theory is that intra-species genetic diversity determines the adaptive potential of any species. This diversity results from the interaction between three factors: the effective population size, natural selection and the rate of recombination. All three factors are influenced by the occurrence of long dormant stages (seed banking or seed persistence), which is an evolutionary bet hedging strategy and a key characteristic of many angiosperms, but also bacteria, fungi or invertebrates. Perhaps surprisingly, this ecological trait has so far been almost ignored in evolutionary genomics. Seed banking is expected to have a fundamental influence on neutral and selective evolutionary processes, and is therefore a key factor to comprehend angiosperm genomic evolution. Theoretical modeling aims to predict the effect of seed banking on patterns of nucleotide diversity. We first adapt for seed banks the two classical mathematical frameworks of population genetics: (1) the backward in time process of the Kingman n-coalescent, and (2) the forward in time diffusion approach. This allows us to derive population genetics quantities and statistics that can be obtained from DNA sequence data. Second, we generate new predictions on neutral diversity and past demographic inference for single and multiple populations under seed banks. Third, we compute the expected effect of seed banks on unlinked (genome wide selection) and linked (gene level selection) sites. Finally, we conclude by suggesting three hypotheses, which can be tested by contrasting polymorphism data in seed banking and non-seed banking species.

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References

  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  CAS  Google Scholar 

  2. Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  3. Blath J, González-Casanova A, Kurt N, Spano D (2013) On the ancestral process of long-range seedbank models. J Appl Probab 50:741–759

    Article  Google Scholar 

  4. Campos JL, Halligan DL, Haddrill PR, Charlesworth B (2014) The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster. Mol Biol Evol 31:1010–1028

    Article  CAS  Google Scholar 

  5. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res 70:155–174

    Article  CAS  Google Scholar 

  7. Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195–205

    Article  CAS  Google Scholar 

  8. Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Roberts & Company Publishers, Greenwood Village

    Google Scholar 

  9. Chen J, Glémin S, Lascoux M (2017) Genetic diversity and the efficacy of purifying selection across plant and animal species. Mol Biol Evol 34:1417–1428

    Article  Google Scholar 

  10. Cohen D (1966) Optimizing reproduction in a randomly varying environment. J. Theor. Biol. 12:119–129

    Article  CAS  Google Scholar 

  11. Corbett-Detig RB, Hartl DL, Sackton TB (2015) Natural selection constrains neutral diversity across a wide range of species. PLoS Biol 13:e1002112

    Article  Google Scholar 

  12. Dann M, Bellot S, Schepella S, Schaefer H, Tellier A (2017) Mutation rates in seeds and seed-banking influence substitution rates across the angiosperm phylogeny. bioRxiv. https://doi.org/10.1101/156398

  13. Ellegren H, Galtier N (2016) Determinants of genetic diversity. Nat Rev Genet 17:422–433

    Article  CAS  Google Scholar 

  14. Evans MEK, Dennehy JJ (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. Q Rev Biol 80:431–451

    Article  Google Scholar 

  15. Evans MEK, Ferriere R, Kane MJ, Venable DL (2007) Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations. Am Nat 169:184–194

    Article  Google Scholar 

  16. Ewens WJ (2004) Mathematical population genetics: I. Theoretical introduction. Springer, Berlin

    Chapter  Google Scholar 

  17. Fenner M, Thompson K (2004) The ecology of seeds, Cambridge University Press, Cambridge

    Google Scholar 

  18. González-Casanova A, Aguirre-von-Wobeser E, Espín G, Servín-González L, Kurt N, Spanò D et al Strong seedbank effects in bacterial evolution. J Theor Biol 356:62–70 (2014)

    Article  Google Scholar 

  19. Gossmann TI, Song BH, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV et al Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol 27:1822–1832 (2010)

    Article  CAS  Google Scholar 

  20. Gossmann TI, Keightley PD, Eyre-Walker A (2012) The effect of variation in the effective population size on the rate of adaptive molecular evolution in eukaryotes. Genome Biol Evol 4:658–667

    Article  Google Scholar 

  21. Griffiths RC (2003) The frequency spectrum of a mutation, and its age, in a general diffusion model. Theor Popul Biol 64:241–251

    Article  CAS  Google Scholar 

  22. Griffiths RC, Tavaré S (1998) The age of a mutation in a general coalescent tree. Stoch. Models 14:273–295

    Article  Google Scholar 

  23. Hairston Jr NG, De Stasio Jr BT (1988) Rate of evolution slowed by a dormant propagule pool. Nature 336:239–242

    Article  Google Scholar 

  24. Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352

    Article  CAS  Google Scholar 

  25. Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294

    Article  CAS  Google Scholar 

  26. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination: Tansley review. New Phytol 171:501–523

    Article  CAS  Google Scholar 

  27. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci 107:5881–5886

    Article  CAS  Google Scholar 

  28. Kaj I, Krone SM, Lascoux M (2001) Coalescent theory for seed bank models. J Appl Probab 38:285–300

    Article  Google Scholar 

  29. Kim Y, Stephan, W (2002) Detecting a local signature of genetic hitchhiking long a recombining chromosome. Genetics 160:765–777

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kingman JFC (1982) On the genealogy of large populations. J Appl Probab 19A:27–43

    Article  Google Scholar 

  31. Kimura M (1955) Stochastic processes and distribution of gene frequencies under natural selection. In: Cold spring harbor symposia on quantitative biology, vol 20. Cold Spring Harbor Laboratory Press, pp 33–53

    Google Scholar 

  32. Kimura M (1955) Random genetic drift in multi-allelic locus. Evolution 9:419–435

    Article  Google Scholar 

  33. Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893–903

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Koopmann B, Müller J, Tellier A, Živković D (2017) Fisher-Wright model with deterministic seed bank and selection. Theor Popul Biol 114:29–39

    Article  Google Scholar 

  35. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  Google Scholar 

  36. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L, Venkat A et al (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10:e1001388

    Article  CAS  Google Scholar 

  37. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119

    Article  CAS  Google Scholar 

  38. Levin DA (1990) The seed bank as a source of genetic novelty in plants. Am. Nat. 135:563–572

    Article  Google Scholar 

  39. Lewontin RC The genetic basis of evolutionary change. Columbia University Press (1974)

    Google Scholar 

  40. Lynch M, Lande R (1998) The critical effective size for a genetically secure population. Anim. Conserv. 1:70–72

    Article  Google Scholar 

  41. Maynard-Smith J, Haigh J (1974) Hitch-hiking effect of a favorable gene. Genet Res 23:23–35

    Article  Google Scholar 

  42. Möst M, Oexle S, Markova S, Aidukaite D, Baumgartner L, Stich HB et al (2015) Population genetic dynamics of an invasion reconstructed from the sediment egg bank. Mol Ecol 24:4074–4093

    Article  Google Scholar 

  43. Nunney L (2002) The effective size of annual plant populations: the interaction of a seed bank with fluctuating population size in maintaining genetic variation. Am Nat 160:195–204

    Article  Google Scholar 

  44. Pease JB, Haak DC, Hahn MW, Moyle LC (2016) Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol 14:e1002379

    Article  Google Scholar 

  45. Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A et al (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515:261–263

    Article  CAS  Google Scholar 

  46. Roselius K, Stephan W, Städler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763

    Article  CAS  Google Scholar 

  47. Salguero-Gómez R (2017) Applications of the fast-slow continuum and reproductive strategy framework of plant life histories. New Phytol 213:1618–1624

    Article  Google Scholar 

  48. Song YSS, Steinrücken M (2012) A simple method for finding explicit analytic transition densities of diffusion processes with general diploid selection. Genetics 190:1117–1129

    Article  Google Scholar 

  49. Templeton AR, Levin DA (1979) Evolutionary consequences of seed pools. Am Nat 114:232–249

    Article  Google Scholar 

  50. Tellier A, Lemaire C (2014) Coalescence 2.0: a multiple branching of recent theoretical developments and their applications. Mol Ecol 23:2637–2652

    Article  Google Scholar 

  51. Tellier A, Brown JKM (2009) The influence of perenniality and seed banks on polymorphism in plant-parasite interactions. Am Nat 174:769–779

    PubMed  Google Scholar 

  52. Tellier A, Laurent SJ, Lainer H, Pavlidis P, Stephan W (2011) Inference of seed bank parameters in two wild tomato species using ecological and genetic data. Proc Natl Acad Sci USA 108:17052–17057

    Article  CAS  Google Scholar 

  53. Turelli M, Schemske DW, Bierzychudek P (2001) Stable two-allele polymorphisms maintained by fluctuating fitnesses and seed banks: protecting the blues in Linanthus parryae. Evolution 55:1283–1298

    Article  CAS  Google Scholar 

  54. Venable DL (1989) Modeling the evolutionary ecology of seed banks. In: Leck MA (ed) Ecology of soil seed banks. Elsevier, Amsterdam, pp 67–87

    Chapter  Google Scholar 

  55. Venable DL, Lawlor L (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46:272–282

    Article  Google Scholar 

  56. Vitalis R, Glémin S, Olivieri I (2004) When genes go to sleep: the population genetic consequences of seed dormancy and monocarpic perenniality. Am Nat 163:295–311

    Article  Google Scholar 

  57. Vy HMT, Kim Y (2015) A Composite-likelihood method for detecting incomplete selective sweep from population genomic data. Genetics 200:633–649

    Article  Google Scholar 

  58. Waterworth WM, Footitt S, Bray CM, Finch-Savage WE, West CE (2016) DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds. Proc Natl Acad Sci 113:9647–9652

    Article  CAS  Google Scholar 

  59. Wright SI, Andolfatto P (2008) The impact of natural selection on the genome: emerging patterns in Drosophila and Arabidopsis. Annu Rev Ecol Evol Syst 39:193–213

    Article  Google Scholar 

  60. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519

    Article  CAS  Google Scholar 

  61. Živković D, Stephan W (2011) Analytical results on the neutral non-equilibrium allele frequency spectrum based on diffusion theory. Theor Popul Biol 79:184–191

    Article  Google Scholar 

  62. Živković D, Tellier A (2012) Germ banks affect the inference of past demographic events. Mol Ecol 21:5434–5446

    Article  Google Scholar 

  63. Živković D, Wiehe T (2008) Second-order moments of segregating sites under variable population size. Genetics 180:341–357

    Article  Google Scholar 

  64. Živković D, Steinrücken M, Song YSS, Stephan W (2015) Transition densities and sample frequency spectra of diffusion processes with selection and variable population size. Genetics 200:601–617

    Article  Google Scholar 

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Acknowledgements

This contribution is supported in part by Deutsche Forschungsgemeinschaft grants TE 809/1 (AT) and STE 325/14 from the Priority Program 1590 (DZ).

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Authors and Affiliations

  1. Section of Population Genetics, Technical University of Munich, Freising, Germany

    Daniel Živković & Aurélien Tellier

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  1. Daniel Živković
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  2. Aurélien Tellier
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Correspondence to Aurélien Tellier .

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Editors and Affiliations

  1. Computational and Systems Biology, John Innes Centre, Norwich, Norfolk, UK

    Richard J. Morris

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Živković, D., Tellier, A. (2018). All But Sleeping? Consequences of Soil Seed Banks on Neutral and Selective Diversity in Plant Species. In: Morris, R. (eds) Mathematical Modelling in Plant Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-99070-5_10

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