Background and aims – Introduced populations can potentially experience strong selection and rapid evolution. While some retrospective studies have shown rapid evolution in introduced populations in the past, few have directly tested for and characterized evolution as it occurs. Here we use an experimental introduction to directly observe and quantify evolution of multiple traits in a plant population introduced to a novel environment.
Methods – We experimentally introduced seeds of the annual plant Brassica rapa L. (Brassicaceae) from a location in southern California into multiple replicated plots in New York. We allowed the populations to naturally evolve for 3 years. Following the resurrection approach, we compared ancestors and descendants planted in common garden conditions in New York in multiple phenotypic traits.
Key results – Within only three generations, there was significant evolution of several morphological, phenological, and fitness traits, as well as substantial variation among traits. Despite selection for larger size during the three years following introduction, there was evolution of smaller size, earlier flowering time, and shorter duration of flowering. Although there were rapid evolutionary changes in traits, descendants did not have greater fitness than ancestors in New York, indicating a lack of evidence for adaptive evolution, at least over the timeframe of the study.
Conclusions – This study found rapid evolution of several morphological and phenological traits, including smaller plant size and shorter time to flowering, following introduction, confirming that evolution can rapidly occur during the early stages of colonization. Many traits evolved in the opposite direction predicted from phenotypic selection analysis, which suggests that the resurrection approach can reveal unanticipated evolutionary changes and can be very useful for studying contemporary evolution.
Agren J., Schemske D. (1994) Evolution of trichome number in a naturalized population of Brassica rapa. The American Naturalist 143: 1–13. https://doi.org/10.1086/285593
Amundsen P.-A., Salonen E., Niva T., Gjelland K.Ø., Præbel K., Sandlund O.T., Knudsen R., Bøhn T. (2012) Invader population speeds up life history during colonization. Biological Invasions 14: 1501–1513. https://doi.org/10.1007/s10530-012-0175-3
Ashworth M.B., Walsh M.J., Flower K.C., Vila-Aiub M.M., Powles S.B. (2016) Directional selection for flowering time leads to adaptive evolution in Raphanus raphanistrum (Wild radish). Evolutionary Applications 9: 619–629. https://doi.org/10.1111/eva.12350
Barrett S.C.H. (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk D.A., Holsinger K.E. (eds) Genetics and Conservation of Rare Plants: 3–30. Oxford, Oxford University Press
Bell G., Gonzalez A. (2009) Evolutionary rescue can prevent extinction following environmental change. Ecological Letters 12: 942–948. https://doi.org/10.1111/j.1461-0248.2009.01350.x
Benjamini Y., Hochberg Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57: 289–300.
Blows M.W., Hoffmann A.A. (2005) A reassessment of genetic limits to evolutionary change. Ecology 86: 1371–1384. https://doi.org/10.1890/04-1209
Bone E., Farres A. (2001) Trends and rates of microevolution in plants. Genetica 112: 165–182. https://doi.org/10.1023/A:1013378014069
Brown M.B., Forsythe A.B. (1974) Robust tests for the equality of variances. Journal of the American Statistical Association 69: 364–367. https://doi.org/10.2307/2285659
Buswell J.M., Moles A.T., Hartley S. (2011) Is rapid evolution common in introduced plant species? Journal of Ecology 99: 214–224. https://doi.org/10.1111/j.1365-2745.2010.01759.x
Campbell L.G., Snow A.A., Ridley C.E. (2006) Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment. Ecological Letters 9: 1198–1209. https://doi.org/10.1111/j.1461-0248.2006.00974.x
Carroll S.P., Jorgensen P.S., Kinnison M.T., Bergstrom C.T., Denison R.F., Gluckman P., Smith T.B., Strauss S.Y., Tabashnik B.E. (2014) Applying evolutionary biology to address global challenges. Science 346: 1245993. https://doi.org/10.1126/science.1245993
Colautti R.I., Lau J.A. (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Molecular Ecology 24: 1999–2017. https://doi.org/10.1111/mec.13162
Dlugosch K.M., Anderson S.R., Braasch J., Cang F.A., Gillette H.D. (2015) The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Molecular Ecology 24: 2095–2111. https://doi.org/10.1111/mec.13183
Dlugosch K.M., Parker I.M. (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449. https://doi.org/10.1111/j.1365-294X.2007.03538.x
Etterson J.R., Franks S.J., Mazer S.J., Shaw R.G., Soper Gorden N.L., Schneider H.E., Weber J.J., Winkler K.J., Weis A.E. (2016) Project baseline: An unprecedented resource to study plant evolution across space and time. American Journal of Botany 103: 164–173. https://doi.org/10.3732/ajb.1500313
Etterson J.R., Shaw R.G. (2001) Constraint to adaptive evolution in response to global warming. Science 294: 151–154. https://doi.org/10.1126/science.1063656
Falconer D.S., Mackay T.F.C. (1996) Introduction to quantitative genetics. 4th Ed. Harlow, Longmans Green.
Farquhar G.D., Ehleringer J.R., Hubick K.T. (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Forsman A., Wennersten L., Karlsson M., Caesar S. (2012) Variation in founder groups promotes establishment success in the wild. Proceedings of the Royal Society B Biological Sciences 279: 2800–2806. https://doi.org/10.1098/rspb.2012.0174
Franks S.J. (2011) Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa. New Phytologist 190: 249–257. https://doi.org/10.1111/j.1469-8137.2010.03603.x
Franks S.J., Avise J.C., Bradshaw W.E., Conner J.K., Etterson J.R., Mazer S.J., Shaw R.G., Weis A.E. (2008a) The resurrection initiative: storing ancestral genotypes to capture evolution in action. Bioscience 58: 870–873. https://doi.org/10.1641/B580913
Franks S.J., Kane N.C., O’Hara N.B., Tittes S., Rest J.S. (2016) Rapid genome-wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools. Molecular Ecology 25: 3622–3631. https://doi.org/10.1111/mec.13615
Franks, S.J., Hamann E., Weis A.E. (2018) Using the resurrection approach to understand contemporary evolution in changing environments. Evolutionary Applications 11: 17–28. https://doi.org/10.1111/eva.12528
Franks S.J., Pratt P.D., Dray F.A., Simms E.L. (2008b) Selection on herbivory resistance and growth rate in an invasive plant. The American Naturalist 171: 678–691. https://doi.org/10.1086/587078
Franks S.J., Sim S., Weis A.E. (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the Natural Academy of Sciences of the United States of America 104: 1278–1282. https://doi.org/10.1073/pnas.0608379104
Franks S.J., Weis A.E. (2008) A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant. Journal of Evolutionary Biology 21: 1321–1334. https://doi.org/10.1111/j.1420-9101.2008.01566.x
Franks S.J., Wheeler G.S., Goodnight C. (2012) Genetic variation and evolution of secondary compounds in native and introduced populations of the invasive plant Melaleuca quinquenervia. Evolution 66: 1398–1412. https://doi.org/10.1111/j.1558-5646.2011.01524.x
Gingerich P.D. (1993) Quantification and comparison of evolutionary rates. American Journal of Science 293A: 453–478. https://doi.org/10.2475/ajs.293.A.453
Gordon S.P., Reznick D., Arendt J.D., Roughton A., Ontiveros Hernandez M.N., Bentzen P., López-Sepulcre A. (2015) Selection analysis on the rapid evolution of a secondary sexual trait. Proceedings of the Royal Society B Biological Sciences 282: 20151244. https://doi.org/10.1098/rspb.2015.1244
Gotanda K.M., Hendry A.P. (2014) Using adaptive traits to consider potential consequences of temporal variation in selection: male guppy colour through time and space. Biological Journal of the Linnean Society 112: 108–122. https://doi.org/10.1111/bij.12261
Grant B.R., Grant P.R (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proceedings of the Royal Society B Biological Sciences 251: 111–117. https://doi.org/10.1098/rspb.1993.0016
Griffith C., Kim E., Donohue K. (2004) Life-history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in North America. American Journal of Botany 91: 837–849. https://doi.org/10.3732/ajb.91.6.837
Griffith T.M., Watson M.A. (2006) Is evolution necessary for range expansion? Manipulating reproductive timing of a weedy annual transplanted beyond its range. The American Naturalist 167: 153–164. https://doi.org/10.1086/498945
Herrel A., Huyghe K., Vanhooydonck B., Backeljau T., Breugelmans K., Grbac I., Van Damme R., Irschick D.J. (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the United States of America 105: 4792–4795. https://doi.org/10.1073/pnas.0711998105
Hovick S.M., Campbell L.G., Snow A.A., Whitney K.D. (2012) Hybridization alters early life-history traits and increases plant colonization success in a novel region. The American Naturalist 179: 192–203. https://doi.org/10.1086/663684
Kettlewell H.B.D. (1958) A survey of the frequencies of Biston betularia (L.)(Lep.) and its melanic forms in Great Britain. Heredity 12: 51–72. https://doi.org/10.1038/hdy.1958.4
Kopp M., Matuszewski S. (2014) Rapid evolution of quantitative traits: theoretical perspectives. Evolutionary Applications 7: 169–191. https://doi.org/10.1111/eva.12127
Leishman M.R., Cooke J., Richardson D.M. (2014) Evidence for shifts to faster growth strategies in the new ranges of invasive alien plants. Journal of Ecology 102: 1451–1461. https://doi.org/10.1111/1365-2745.12318
Levitan M. (2003) Climatic factors and increased frequencies of “southern” chromosome forms in natural populations of Drosophila robusta. Evolutionary Ecology Research 5: 597–604.
Maron J., Vilà M., Bommarco R., Elmendorf S., Beardsley P. (2004) Rapid evolution of an invasive plant. Ecology 74: 261–280. https://doi.org/10.1890/03-4027
Nevo E., Fu Y.-B., Pavlicek T., Khalifa S., Tavasi M., Beiles A. (2012) Evolution of wild cereals during 28 years of global warming in Israel. Proceedings of the National Academy of Sciences of the United States of America 109: 3412–3415. https://doi.org/10.1073/pnas.1121411109
Novy A., Flory S.L., Hartman J.M. (2013) Evidence for rapid evolution of phenology in an invasive grass. Journal of Evolutionary Biology 26: 443–450. https://doi.org/10.1111/jeb.12047
Palumbi S. (2001) Humans as the world’s greatest evolutionary force. Science 293: 1786–1790. https://doi.org/10.1126/science.293.5536.1786
Pitchers W., Wolf J.B., Tregenza T., Hunt J., Dworkin I. (2014) Evolutionary rates for multivariate traits: the role of selection and genetic variation. Philosophical Transactions of the Royal Society B Biological Sciences 369: 20130252. https://doi.org/10.1098/rstb.2013.0252
Prentis P.J., Wilson J.R.U., Dormontt E.E., Richardson D.M., Lowe A.J. (2008) Adaptive evolution in invasive species. Trends in Plant Science 13: 288–294. https://doi.org/10.1016/j.tplants.2008.03.004
Reznick D.N., Ghalambor C.K. (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112: 183–198. https://doi.org/10.1023/A:1013352109042
Reznick D.N., Shaw F.H., Rodd F.H., Shaw R.G. (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275: 1934–1937. https://doi.org/10.1126/science.275.5308.1934
Ridley C.E., Ellstrand N.C. (2010) Rapid evolution of morphology and adaptive life history in the invasive California wild radish (Raphanus sativus) and the implications for management. Evolutionary Applications 3: 64–76. https://doi.org/10.1111/j.1752-4571.2009.00099.x
Sekor M.R., Franks S.J. (2018) An experimentally introduced population of Brassica rapa (Brassicaceae). 1. Phenotypic selection over three years following colonization of a novel environment. Plant Ecology and Evolution 151: 209–218. https://doi.org/10.5091/plecevo.2018.1354
Snedecor G.W., Cochran W.G. (1980) Statistical methods. Ames, Iowa State University Press.
Stuart Y.E., Campbell T.S., Hohenlohe P.A., Reynolds R.G., Revell L.J., Losos J.B. (2014) Rapid evolution of a native species following invasion by a congener. Science 346: 463–466. https://doi.org/10.1126/science.1257008
Thompson J.N. (2013) Relentless evolution. Chicago, The University of Chicago Press.
Van Buskirk J., Willi Y. (2006) The change in quantitative genetic variation with inbreeding. Evolution 60: 2428–2434. https://doi.org/10.1111/j.0014-3820.2006.tb01879.x
Vandepitte K., de Meyer T., Helsen K., van Acker K., Roldán‐Ruiz I., Mergeay J., Honnay O. (2014) Rapid genetic adaptation precedes the spread of an exotic plant species. Molecular Ecology 23: 2157–2164. https://doi.org/10.1111/mec.12683
Walsh B., Blows M.W. (2009) Abundant genetic variation + strong selection = multivariate genetic constraints: a geometric view of adaptation. The Annual Review of Ecology, Evolution, and Systematics 40: 41–59. https://doi.org/10.1146/annurev.ecolsys.110308.120232
Walsh M.R., Reznick D.N. (2011) Experimentally induced life-history evolution in a killifish in response to the introduction of guppies. Evolution 65: 1021–1036. https://doi.org/10.1111/j.1558-5646.2010.01188.x
Whalon M., Mota-Sanchez D., Hollingworth R. (2008) Global pesticide resistance in arthropods. Wallingford, CABI. https://doi.org/10.1079/9781845933531.0000
Williams P.H., Hill C.B. (1986) Rapid-cycling populations of Brassica. Science 232: 1385–1389. https://doi.org/10.1126/science.232.4756.1385
For material published before 1 January 2019, all rights are reserved. Copyright holders are Meise Botanic Garden and the Royal Botanical Society of Belgium. Permission to use this material must always be obtained from the Editor in chief, via the Editorial Office.
For further information on access, permissions and re-use of papers published in Plant Ecology and Evolution, please read our Open Access policy.