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Rapid evolution with generation overlap: the double-edged effect of dormancy

Abstract

In life histories with generation overlap, selection that acts differently on different life-stages can produce reservoirs of genetic variation, for example, in long-lived iteroparous adults or long-lived dormant propagules. Such reservoirs provide “migration from the past” to the current population, and depending on the trend of environmental change, they have the potential either to slow adaptive evolution or accelerate it by re-introducing genotypes not affected by recent selection (e.g., through storage effect in a fluctuating environment). That is, the effect of generation overlap is a “double-edged sword,” with each edge cutting in a different direction. Here, we use sexual (quantitative trait) and asexual (clonal) models to explore the effects of generation overlap on adaptive evolution in a fluctuating environment, either with or without a trend in the mean environment state. Our analyses show that when environmental stochasticity scaled by strength of selection is intermediate and when the trend in mean environment is slow, intermediate values of generation overlap can maximize the rate of response to selection and minimize the adaptation lag between the trait mean and the environmental trend. Otherwise, increased generation overlap results in smaller selection response and larger adaptation lag. In the former case, low generation overlap results in low heritable trait variance, while high generation overlap increases the “migration load” from the past. Therefore, to understand the importance of rapid evolution and eco-evolutionary dynamics in the wild for organisms with overlapping generations, we need to understand the interaction of generation overlap, environmental stochasticity, and strength of selection.

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References

  1. Abrams PA, Tucker CM, Gilbert B (2013) Evolution of the storage effect. Evolution 67:315–327

    PubMed  Google Scholar 

  2. Alexander HK, Martin G, Martin OY, Bonhoeffer S (2014) Evolutionary rescue: linking theory for conservation and medicine. Evol Appl 7:1161–1179

    PubMed  PubMed Central  Google Scholar 

  3. Barfield M, Holt RD, Gomulkiewicz R (2011) Evolution in stage-structured populations. Am Nat 177:397–409

    PubMed  PubMed Central  Google Scholar 

  4. Barton NH, Etheridge AM, Véber A (2017) The infinitesimal model: definition, derivation, and implications. Theor Popul Biol 118:50–73

    CAS  PubMed  Google Scholar 

  5. Baumgartner MF, Tarrant AM (2017) The physiology and ecology of diapause in marine copepods. Annu Rev Mar Sci 9:387–411

    Google Scholar 

  6. Bell G (2010) Fluctuating selection: the perpetual renewal of adaptation in variable environments. Phil Trans R Soc B 365:87–97

    PubMed  Google Scholar 

  7. Bell G (2017) Evolutionary rescue. Annu Rev Ecol Evol Syst 48:605–627

    Google Scholar 

  8. Bolnick DI, Nosil P (2007) Natural selection in populations subject to a migration load. Evolution 61:2229–2243

    PubMed  Google Scholar 

  9. Brendonck L, De Meester L (2003) Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84

    Google Scholar 

  10. Bridle JR, Polechová J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecol Lett 13:485–494

    PubMed  Google Scholar 

  11. Brown JS, Venable DL (1986) Evolutionary ecology of seed-bank annuals in temporally varying environments. Am Nat 127:31–47

    Google Scholar 

  12. Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP (2009) Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytol 181:463–470

    PubMed  Google Scholar 

  13. Bulmer MG (1980) The Mathematical Theory of Quantitative Genetics. Clarendon Press, Oxford

    Google Scholar 

  14. Bürger R, Lynch M (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution 49:151–163

    Google Scholar 

  15. Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biology 8:e1000357

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  17. Cohen D, Levin SA (1991) Dispersal in patchy environments: the effects of temporal and spatial structure. Theor Popul Biol 39:63–99

    Google Scholar 

  18. Dempster ER (1955) Maintenance of genetic heterogeneity. Pages 25–32 in Cold Spring Harbor Symposia on Quantitative Biology. Vol. 20. Cold Spring Harbor Laboratory Press

  19. Doebeli M, Dieckmann U (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am Nat 156:S77–S101

    PubMed  Google Scholar 

  20. Ellegaard M, Ribeiro S (2018) The long-term persistence of phytoplankton resting stages in aquatic ‘seed banks’. Biol Rev 93:166–183

    PubMed  Google Scholar 

  21. Ellner S, Hairston NG Jr (1994) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. Am Nat 143:403–417

    Google Scholar 

  22. Ellner S, Sasaki A (1996) Patterns of genetic polymorphism maintained by fluctuating selection with overlapping generations. Theor Popul Biol 50:31–65

    CAS  PubMed  Google Scholar 

  23. Ellner SP, Hairston NG Jr, Kearns CM, Babaï D (1999) The roles of fluctuating selection and long-term diapause in microevolution of diapause timing in a freshwater copepod. Evolution 53:111–122

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  25. Gomulkiewicz R, Holt RD (1995) When does evolution by natural selection prevent extinction? Evolution 49:201–207

    PubMed  Google Scholar 

  26. Gyllström M, Hansson L-A (2004) Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquat Sci 66:274–295

    Google Scholar 

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

    Google Scholar 

  28. Hairston NG Jr, Ellner S, Kearns CM (1996a) Overlapping generations: the storage effect and the maintenance of biotic diversity. In: Rhodes OE Jr, Chesser RK, Smith MH (eds.) Population Dynamics in Ecological Space and Time. University of Chicago Press, Chicago, pp 109–145

    Google Scholar 

  29. Hairston NG Jr, Kearns CM, Ellner SP (1996b) Phenotypic variation in a zooplankton egg bank. Ecology 77:2382–2392

    Google Scholar 

  30. Haldane JBS, Jayakar SD (1963) Polymorphism due to selection of varying direction. J Genet 58:237–242

    Google Scholar 

  31. Hastings A (2004) Transients: the key to long-term ecological understanding? Trends Ecol Evol 19:39–45

    PubMed  Google Scholar 

  32. Hedrick PW (1995) Genetic polymorphism in a temporally varying environment: effects of delayed germination or diapause. Heredity 75:164–170

    Google Scholar 

  33. Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences II. The “handicap” principle. Evolution 45:1431–1442

    PubMed  Google Scholar 

  34. Kinnison MT, Hairston NG Jr (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct Ecol 21:444–454

    Google Scholar 

  35. Kopp M, Matuszewski S (2014) Rapid evolution of quantitative traits: theoretical perspectives. Evol Appl 7:169–191

    PubMed  Google Scholar 

  36. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130

    CAS  PubMed  Google Scholar 

  37. Levin SA, Cohen D, Hastings A (1984) Dispersal strategies in patchy environments. Theor Popul Biol 26:165–191

    Google Scholar 

  38. Ludwig D, Levin SA (1991) Evolutionary stability of plant communities and the maintenance of multiple dispersal types. Theor Popul Biol 40:285–307

    Google Scholar 

  39. Lynch M, Lande R (1993) Evolution and extinction in response to environmental change. In: Kareiva PM, Kingsolver JG, Huey RB (eds.) Biotic Interactions and Global Change. Sinauer Associates Inc., Sunderland, pp 234–250

    Google Scholar 

  40. Messer PW, Ellner SP, Hairston NG Jr (2016) Can population genetics adapt to rapid evolution? Trends Genet 32:408–418

    CAS  PubMed  Google Scholar 

  41. Miller ET, Klausmeier CA (2017) Evolutionary stability of coexistence due to the storage effect in a two-season model. Theor Ecol 10:91–103

    Google Scholar 

  42. Miner BE, De Meester L, Pfrender ME, Lampert W, Hairston NG Jr (2012) Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proc R Soc B 279:1873–1882

    PubMed  Google Scholar 

  43. Nuismer SL, Doebeli M, Browning D (2005) The coevolutionary dynamics of antagonistic interactions mediated by quantitative traits with evolving variances. Evolution 59:2073–2082

    CAS  PubMed  Google Scholar 

  44. Orive ME, Barfield M, Fernandez C, Holt RD (2017) Effects of clonal reproduction on evolutionary lag and evolutionary rescue. Am Nat 190:469–490

    PubMed  Google Scholar 

  45. Pantel JH, Duvivier C, De Meester L (2015) Rapid local adaptation mediates zooplankton community assembly in experimental mesocosms. Ecol Lett 18:992–1000

    PubMed  Google Scholar 

  46. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria

  47. Rees M (1996) Evolutionary ecology of seed dormancy and seed size. Phil Trans R Soc B 351:1299–1308

    Google Scholar 

  48. Rees M, Ellner SP (in press) Why so variable: can genetic variance in flowering thresholds be maintained by fluctuating selection? Am Nat

  49. Sasaki A, Ellner S (1997) Quantitative genetic variance maintained by fluctuating selection with overlapping generations: variance components and covariances. Evolution 51:682–696

    PubMed  Google Scholar 

  50. Snyder RE, Adler PB (2011) Coexistence and coevolution in fluctuating environments: can the storage effect evolve? Am Nat 178:E76–E84

    PubMed  Google Scholar 

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

    Google Scholar 

  52. Turelli M (2017) Fisher’s infinitesimal model: a story for the ages. Theor Popul Biol 118:46–49

    PubMed  Google Scholar 

  53. Turelli M, Barton NH (1994) Genetic and statistical analyses of strong selection on polygenic traits: what, me normal? Genetics 138:913–941

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 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

    CAS  PubMed  Google Scholar 

  55. Walsh B, Lynch M (2018) Evolution and Selection of Quantitative Traits. Oxford University Press, Oxford

    Google Scholar 

Download references

Acknowledgements

We thank two anonymous referees for detailed and helpful comments on the original manuscript.

Funding

M.Y. was supported by the Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Scientific Research (KAKENHI) 15H02642, 16K18618, 16H04846, and 18H02509 and by Hakubi Center for Advanced Research and John Mung Program of Kyoto University. N.G.H. was supported by USDA National Institute of Food and Agriculture, Hatch Grant 1007884, and by Eawag, the Swiss Federal Institute of Aquatic Science and Technology, while this paper was being prepared for publication. M.R. was supported by NERC-NE/K014048/1. S.P.E. was supported by US National Science Foundation grant DEB 1353039.

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Correspondence to Masato Yamamichi.

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Yamamichi, M., Hairston, N.G., Rees, M. et al. Rapid evolution with generation overlap: the double-edged effect of dormancy. Theor Ecol 12, 179–195 (2019). https://doi.org/10.1007/s12080-019-0414-7

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Keywords

  • Environmental stochasticity
  • Evolutionary lag
  • Fluctuating selection
  • Moving optimum
  • Standing genetic variation
  • Storage effect