Abstract
A capacity to predict the spread rate of populations is critical for understanding the impacts of climate change and invasive species. Despite sophisticated theory describing how populations spread, the prediction of spread rate remains a formidable challenge. As well as the inherent stochasticity in the spread process, spreading populations are subject to strong evolutionary forces (operating on dispersal and reproductive rates) that can cause accelerating spread. Despite these strong evolutionary forces, serial founder events and drift on the expanding range edge mean that evolutionary trajectories in the invasion vanguard may be highly stochastic. Here I develop a model of spatial spread in continuous space that incorporates evolution of continuous traits under a quantitative genetic model of inheritance. I use this model to investigate the potential role of evolution on the variation in spread rate between replicate model realisations. Models incorporating evolution exhibited more than four times the variance in spread rate across replicate invasions compared with non-evolving scenarios. Results suggest that the majority of this increase in variation is driven by evolutionary stochasticity on the invasion front rather than initial founder events: in many cases evolutionary stochasticity on the invasion front contributed more than 90 % of the variance in spread rate over 30 generations. Our uncertainty around predicted spread rates—whether for invasive species or those shifting under climate change—may be much larger than we expect when the spreading population contains heritable variation in rates of dispersal and reproduction.
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References
Benichou O, Calvez V, Meunier N, Voituriez R (2012) Front acceleration by dynamic selection in Fisher population waves. Phys Rev E 86(4):041908. http://pre.aps.org/abstract/PRE/v86/i4/e041908
Beverton RJH, Holt SJ (1957) On the dynamics of exploited fish populations, vol 19. UK Ministry of Agriculture
Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19(1):12–20. doi:10.1111/j.1420-9101.2005.00995.x, http://www.ncbi.nlm.nih.gov/pubmed/16405572
Bocedi G, Palmer SC, Pe’er G, Heikkinen RK, Matsinos YG, Watts K, Travis JM (2014) RangeShifter: a platform for modelling spatial eco-evolutionary dynamics and species’ responses to environmental changes. Methods Ecol Evol 5(4):388–396. doi:10.1111/2041-210X.12162, http://doi.wiley.com/10.1111/2041-210X.12162
Burton OJ, Travis JMJ, Phillips BL (2010) Trade-offs and the evolution of life-histories during range expansion. Ecol Lett 13:1210–1220
Clark JS, Fastie C, Hurtt G, Jackson ST, Johnson C, King GA, Lewis M, Lynch J, Pacala S, Prentice C, Schupp EW, Webb T III, Wyckoff P, Webb T, King A (1998) Reid’s paradox of rapid plant migration. BioScience 48(1):13–24
Ellner S, Schreiber S (2012) Temporally variable dispersal and demography can accelerate the spread of invading species. Theor Popul Biol 82(4):283–298. http://www.sciencedirect.com/science/article/pii/S0040580912000445, arXiv:1106.1612v2
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 22:347–351
Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Ann Rev Ecol Evol Syst 40(1):481–501. doi:10.1146/annurev.ecolsys.39.110707.173414, http://arjournals.annualreviews.org
Fisher RA (1937) The wave advance of advantageous genes. Ann Eugen 7(355–369):355–369
Hallatschek O, Nelson DR (2008) Gene surfing in expanding populations. Theor Popul Biol 73(1):158–170. doi:10.1016/j.tpb.2007.08.008, http://www.ncbi.nlm.nih.gov/pubmed/17963807
Hallatschek O, Hersen P, Ramanathan S, Nelson DR (2007) Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci USA 104(50):19:926–930. doi:10.1073/pnas.0710150104, http://www.pubmedcentral.nih.gov
Hastings A (1996) Models of spatial spread: a synthesis. Biol Conserv 78(1–2):143–148. ¡Go to ISI¿://A1996VP46800012
Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U, Melbourne BA, Moore K, Taylor C, Thomson D (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101
Hengeveld R (1989) Dynamics of biological invasions. Chapman and Hall, New York
Klopfstein S, Currat M, Excoffier L (2006) The fate of mutations surfing on the wave of range expansion. Mol Biol Evol 23(3):482–490
Kot M, Lewis MA, VandenDriessche P, Van Den Driessche P (1996) Dispersal data and the spread of invading organisms. Ecology 77(7):2027–2042. http://www.esajournals.org
Kubisch A, Fronhofer Ea, Poethke HJ, Hovestadt T (2013) Kin competition as a major driving force for invasions. Am Nat 181(5):700–706. doi:10.1086/670008, http://www.jstor.org
Lewis M (2000) Spread rate for a nonlinear stochastic invasion. J Math Biol 41:430–454. http://link.springer.com/article/10.1007/s002850000022
Lewis M, Pacala S (2000) Modeling and analysis of stochastic invasion processes. J Math Biol 41:387–429. http://link.springer.com/article/10.1007/s002850000050
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland
Melbourne Ba, Hastings A (2009) Highly variable spread rates in replicated biological invasions: fundamental limits to predictability. Science (New York, NY) 325(5947):1536–1539. doi:10.1126/science.1176138, http://www.ncbi.nlm.nih.gov/pubmed/19762641
Neubert MG, Kot M, Lewis Ma (2000) Invasion speeds in fluctuating environments. Proc Biol Sci R Soc 267(1453):1603–1610. doi:10.1098/rspb.2000.1185, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1690727&tool=pmcentrez&rendertype=abstract
Orlando Pa, Gatenby Ra, Brown JS (2013) Tumor evolution in space: the effects of competition colonization tradeoffs on tumor invasion dynamics. Front Oncol 3:1–12. doi:10.3389/fonc.2013.00045, http://www.frontiersin.org
Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L (2013) On the accumulation of deleterious mutations during range expansions. Mol Ecol 22(24):5972–5982. doi:10.1111/mec.12524, http://www.ncbi.nlm.nih.gov/pubmed/24102784
Peischl S, Kirkpatrick M, Excoffier L (2015) Expansion load and the evolutionary dynamics of a species range. Am Nat (in press)
Perkins TA (2012) Evolutionarily labile species interactions and spatial spread of invasive species. Am Nat 179:E37–E54
Perkins TA, Phillips BL, Baskett ML, Hastings A (2013) Evolution of dispersal and life-history interact to drive accelerating spread of an invasive species. Ecol Lett (in press). doi:10.1111/ele.12136
Phillips BL (2009) The evolution of growth rates on an expanding range edge. Biol Lett 5(6):802–804. doi:10.1098/rsbl.2009.0367
Phillips BL, Brown GP, Travis JMJ, Shine R (2008) Reid’s paradox revisited: the evolution of dispersal kernels during range expansion. Am Nat 172(Supp):S34–S48, doi:10.1086/588255, http://www.ncbi.nlm.nih.gov/pubmed/18554142
Phillips B, Brown G, Shine R (2010) Life-history evolution in range-shifting populations. Ecology 91(6):1617–1627. http://www.esajournals.org/doi/abs/10.1890/09-0910.1?ai=rv&af=R
R Development Core Team (2012) R: a language and environment for statistical computing. http://www.r-project.org
Roughgarden JE (1979) Theory of poulation genetics and evolutionary ecology: an introduction. Macmillan, New York
Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution, and biogeography
Schreiber SJ, Ryan ME (2011) Invasion speeds for structured populations in fluctuating environments. Theor Ecol 4(4):423–434. doi:10.1007/s12080-010-0098-5, http://link.springer.com
Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, Oxford
Shine R, Brown GP, Phillips BL (2011) An evolutionary process that assembles phenotypes through space rather than through time. PNAS 108:5708–5711. doi:10.1073/pnas.1018989108
Skellam J (1951) Random dispersal in theoretical populations. Biometrika 38(1):196–218. http://www.springerlink.com/index/13G436H7L4UX38QU.pdf
Slatkin M, Excoffier L (2012) Serial founder effects during range expansion: a spatial analog of genetic drift. Genetics 191(1):171–181. doi:10.1534/genetics.112.139022, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3338258&tool=pmcentrez&rendertype=abstract
Snyder RE (2003) How demographic stochasticity can slow biological invasions. Ecology 84(5):1333–1339. doi:10.1890/0012-9658(2003)084[1333:HDSCSB]2.0.CO;2
Stephens P, Sutherland W (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 17(99):401–405. http://www.sciencedirect.com/science/article/pii/S0169534799016845
Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8(8):895–908. doi:10.1111/j.1461-0248.2005.00787.x, http://blackwell-synergy.com
Tobin PC, Whitmire SL, Johnson DM, Bjørnstad ON, Liebhold AM (2007) Invasion speed is affected by geographical variation in the strength of Allee effects. Ecol Lett 10(1):36–43. doi:10.1111/j.1461-0248.2006.00991.x, http://www.ncbi.nlm.nih.gov/pubmed/17204115
Travis JMJ, Dytham C (2002) Dispersal evolution during invasions. Evol Ecol Res 4:1119–1129
Travis JMJ, Münkemüller T, Burton OJ, Best A, Dytham C, Johst K (2007) Deleterious mutations can surf to high densities on the wave front of an expanding population. Mol Biol Evol 24(10):2334–2343
van Ditmarsch D, Boyle KE, Sakhtah H, Oyler JE, Nadell CD, Déziel E, Dietrich LE, Xavier JB (2013) Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria. Cell Rep 4:697–708. doi:10.1016/j.celrep.2013.07.026, http://linkinghub.elsevier.com/retrieve/pii/S2211124713003884
Acknowledgments
The idea for this paper came whilst preparing a talk for a conference on “Biological invasions and evolutionary biology, stochastic and deterministic models” in Lyon, 2013. So I thank the organisers of the conference—Jean Bérard, Vincent Calvez, and Gaël Raoul—for both the conference and their invitation. I also thank Wayne Mallet and Jeremy Vanderwal for ongoing technical support around High Performance Computing. Funding for this work was provided by the Australian Research Council (DP1094646).
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Phillips, B.L. Evolutionary processes make invasion speed difficult to predict. Biol Invasions 17, 1949–1960 (2015). https://doi.org/10.1007/s10530-015-0849-8
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DOI: https://doi.org/10.1007/s10530-015-0849-8