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
Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709
Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Elsevier, Amsterdam
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
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
Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303
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
Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 10:195–205
Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Roberts & Company Publishers, Greenwood Village
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
Cohen D (1966) Optimizing reproduction in a randomly varying environment. J. Theor. Biol. 12:119–129
Corbett-Detig RB, Hartl DL, Sackton TB (2015) Natural selection constrains neutral diversity across a wide range of species. PLoS Biol 13:e1002112
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
Ellegren H, Galtier N (2016) Determinants of genetic diversity. Nat Rev Genet 17:422–433
Evans MEK, Dennehy JJ (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. Q Rev Biol 80:431–451
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
Ewens WJ (2004) Mathematical population genetics: I. Theoretical introduction. Springer, Berlin
Fenner M, Thompson K (2004) The ecology of seeds, Cambridge University Press, Cambridge
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)
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)
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
Griffiths RC (2003) The frequency spectrum of a mutation, and its age, in a general diffusion model. Theor Popul Biol 64:241–251
Griffiths RC, Tavaré S (1998) The age of a mutation in a general coalescent tree. Stoch. Models 14:273–295
Hairston Jr NG, De Stasio Jr BT (1988) Rate of evolution slowed by a dormant propagule pool. Nature 336:239–242
Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352
Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination: Tansley review. New Phytol 171:501–523
Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci 107:5881–5886
Kaj I, Krone SM, Lascoux M (2001) Coalescent theory for seed bank models. J Appl Probab 38:285–300
Kim Y, Stephan, W (2002) Detecting a local signature of genetic hitchhiking long a recombining chromosome. Genetics 160:765–777
Kingman JFC (1982) On the genealogy of large populations. J Appl Probab 19A:27–43
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
Kimura M (1955) Random genetic drift in multi-allelic locus. Evolution 9:419–435
Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893–903
Koopmann B, Müller J, Tellier A, Živković D (2017) Fisher-Wright model with deterministic seed bank and selection. Theor Popul Biol 114:29–39
Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460
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
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119
Levin DA (1990) The seed bank as a source of genetic novelty in plants. Am. Nat. 135:563–572
Lewontin RC The genetic basis of evolutionary change. Columbia University Press (1974)
Lynch M, Lande R (1998) The critical effective size for a genetically secure population. Anim. Conserv. 1:70–72
Maynard-Smith J, Haigh J (1974) Hitch-hiking effect of a favorable gene. Genet Res 23:23–35
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
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
Pease JB, Haak DC, Hahn MW, Moyle LC (2016) Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol 14:e1002379
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
Roselius K, Stephan W, Städler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763
Salguero-Gómez R (2017) Applications of the fast-slow continuum and reproductive strategy framework of plant life histories. New Phytol 213:1618–1624
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
Templeton AR, Levin DA (1979) Evolutionary consequences of seed pools. Am Nat 114:232–249
Tellier A, Lemaire C (2014) Coalescence 2.0: a multiple branching of recent theoretical developments and their applications. Mol Ecol 23:2637–2652
Tellier A, Brown JKM (2009) The influence of perenniality and seed banks on polymorphism in plant-parasite interactions. Am Nat 174:769–779
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
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
Venable DL (1989) Modeling the evolutionary ecology of seed banks. In: Leck MA (ed) Ecology of soil seed banks. Elsevier, Amsterdam, pp 67–87
Venable DL, Lawlor L (1980) Delayed germination and dispersal in desert annuals: escape in space and time. Oecologia 46:272–282
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
Vy HMT, Kim Y (2015) A Composite-likelihood method for detecting incomplete selective sweep from population genomic data. Genetics 200:633–649
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
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
Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519
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
Živković D, Tellier A (2012) Germ banks affect the inference of past demographic events. Mol Ecol 21:5434–5446
Živković D, Wiehe T (2008) Second-order moments of segregating sites under variable population size. Genetics 180:341–357
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
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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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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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DOI: https://doi.org/10.1007/978-3-319-99070-5_10
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