FOUNDATIONS OF INVASION GENETICS
THE BAKER AND STEBBINS LEGACY
Spencer C. H. Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2 Canada
Search for more papers by this authorSpencer C. H. Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2 Canada
Search for more papers by this authorSpencer C. H. Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2 Canada
Search for more papers by this authorRobert I. Colautti
Department of Biology, Queen's University, Kingston, ON, K7L 3N6 Canada
Search for more papers by this authorKatrina M. Dlugosch
Department of Ecology and Evolutionary Biology, University of Arizona, PO Box 210088, Tucson, AZ, 85721 USA
Search for more papers by this authorLoren H. Rieseberg
Department of Botany, University of British Columbia, 1316–6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada
Department of Biology, Indiana University, Bloomington, IN, 47405 USA
Search for more papers by this authorSummary
Invasion genetics is a relatively new discipline that investigates patterns of genetic variation in populations of invasive species and their ecological and evolutionary consequences. Evolutionary biologists have a long-standing interest in colonizing species, owing to their short life cycles and widespread distributions, but not until publication of The Genetics of Colonizing Species (1965), edited by H.G. Baker and G.L. Stebbins, was a synthesis on the genetics and evolution of colonizers available. Here, I make the case that the Baker and Stebbins volume is the foundational document for invasion genetics, and in conjunction with the increased use of genetic markers and development of invasion biology, resulted in the birth of this new field over the past two decades. I consider the historical origins and legacy of the Baker and Stebbins volume and review some of the key issues that were addressed. I provide biographical sketches of the two editors, emphasizing their contrasting backgrounds and personalities. I review examples from my own work on plant invasions that are relevant to issues discussed by contributors to the volume. These include the following: determinants of invasion success, life history trade-offs, generalist vs. specialist strategies, general-purpose genotypes, adaptive phenotypic plasticity, mating systems and the influence of bottlenecks on genetic variation. I conclude by posing several key questions in invasion genetics and argue that one of the main challenges that the area faces is to integrate experimental field studies of the ecology and demography of populations with the largely descriptive approaches that have tended to dominate most research to date.
REFERENCES
- Ahern RG, Landis DA, Reznicek AA, Schemske DW (2010) Spread of exotic plants in the landscape: the role of time, growth habit, and history of invasiveness. Biological Invasions, 12, 3157–3169.
- Allard RW, Babbel GR, Clegg MT, Kahler AL (1972) Evidence for coadaptation in Avena barbata . Proceedings of the National Academy of Sciences of the United States of America, 69, 3043–3048.
- Ally D, Ritland K, Otto SP (2008) Can clone size serve as a proxy for clone age? An exploration using microsatellite divergence in Populus tremuloides . Molecular Ecology, 17, 4897–4911.
- Andow DA, Kareiva PM, Levin SA, Okubo A (1990) Spread of invading organisms. Landscape Ecology, 4, 177–188.
- Babcock EB, Stebbins GL Jr (1938) The American species of Crepis: their inter-relations and distribution as affected by polyploidy. Carnegie Institute of Washington Publication No 504. Washington, District of Columbia.
- Baker HG (1948) Stages in invasion and replacement by species of Melandrium . Journal of Ecology, 36, 96–119.
- Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution, 9, 347–349.
- Baker HG (1965) Characteristics and modes of origin of weeds. In: The Genetics of Colonizing Species (eds HG Baker, GL Stebbins), pp. 147–168. Academic Press, New York.
- Baker HG (1967) Support for Baker's Law – As a rule. Evolution, 21, 853–856.
- Baker HG (1986) Patterns of plant invasion in North America. In: Ecology of Biological Invasions of North America Ecological Studies 58 (eds HA Mooney, JA Drake), pp. 44–57. Springer-Verlag, New York.
- HG Baker, GL Stebbins (eds) (1965) The Genetics of Colonizing Species. Academic Press, New York.
- Barrett SCH (1980) Sexual reproduction in Eichhornia crassipes (water hyacinth) II. Seed production in natural populations. Journal of Applied Ecology, 17, 113–124.
- Barrett SCH (1983) Crop mimicry in weeds. Economic Botany, 37, 255–282.
- Barrett SCH (1988) Genetics and evolution of agricultural weeds. In: Weed Management in Agroecosystems: Ecological Approaches (eds M Altieri, MZ Liebman), pp. 57–75. CRC Press Inc., Boca Raton, Florida.
-
Barrett SCH (1992) Genetics of weed invasions. In: Applied Population Biology (eds SK Jain, L Botsford), pp. 91–119. Wolfgang Junk, Netherlands.
10.1007/978-0-585-32911-6_5 Google Scholar
- Barrett SCH (2001) The Bakers and Stebbins era comes to a close. Evolution, 55, 2371–2374.
- Barrett SCH (2011) Why reproductive systems matter for the invasion biology of plants. In: Fifty Years of Invasion Ecology The Legacy of Charles Elton (ed. D Richardson), pp. 195–210. Wiley-Blackwell, Oxford.
- Barrett SCH, Richardson BJ (1986) Genetic attributes of invading species. In: Ecology of Biological Invasions: An Australian Perspective (eds RH Groves, JJ Burdon), pp. 21–23. Australian Academy of Science, Canberra.
- Barrett SCH, Seaman DE (1980) The weed flora of Californian rice fields. Aquatic Botany, 9, 351–376.
- Barrett SCH, Shore JS (1987) Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution, 41, 340–354.
- Barrett SCH, Shore JS (1989) Isozyme variation in colonizing plants. In: Isozymes in Plant Biology (eds D Soltis, P Soltis), pp. 106–126. Dioscorides Press, Portland, Oregon.
- Barrett SCH, Strother JL (1978) The taxonomy and natural history of Bacopa (Scrophulariaceae) in California. Systematic Botany, 3, 408–419.
- Barrett SCH, Morgan MT, Husband BC (1989) The dissolution of a complex genetic polymorphism: the evolution of self-fertilization in tristylous Eichhornia paniculata (Pontederiaceae). Evolution, 41, 1398–1416.
- Bobiwash K, Schultz ST, Schoen DJ (2013) Somatic deleterious mutation rate in a woody plant: estimation from phenotypic data. Heredity, 111, 338–344.
- Brown AHD (1979) Enzyme polymorphism in plant populations. Theoretical Population Biology, 15, 1–42.
- Brown AHD (1983) Multilocus organization of plant populations. In: Population Biology and Evolution (eds K Wohrmann, V Loescheke), pp. 159–169. Springer-Verlag, Berlin.
- Brown AHD, Burdon JJ (1983) Multilocus diversity in an outbreeding weed, Echium plantagineum L. Australian Journal of Biological Sciences, 36, 503–509.
- Brown AHD, Marshall DR (1981) Evolutionary changes accompanying colonization in plants. In: Evolution Today: Proceedings of the Second International Congress of Systematic and Evolutionary Biology (eds GGT Scudder, JL Reveal), pp. 351–363. Carnegie-Mellon University, Pittsburgh, Pennsylvania.
- Brown JE, Stepien CA (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns. Molecular Ecology, 18, 64–79.
- Burns JN, Ashman T-L, Steets JA, Harmon-Threatt A, Knight TM (2011) A phylogenetically controlled analysis of the roles of reproductive traits in plant invasions. Oecologia, 166, 1009–1017.
- Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? Trends in Ecology and Evolution, 21, 369–374.
- Carroll SP, Hendry AP, Reznick DN, Fox CW (2007) Evolution on ecological time scales. Functional Ecology, 21, 387–393.
- Cheptou P-O (2012) Clarifying Baker's Law. Annals of Botany, 109, 633–641.
- Cheptou P-O, Lepart J, Escarre J (2002) Mating system variation along a successional gradient in the allogamous colonizing plant Crepis sancta (Asteraceae). Journal of Evolutionary Biology, 15, 753–762.
- Chew MK (2011) Invasion biology: historical precedents. In: Encyclopaedia of Biological Invasions (eds D Simberloff & M Rejmánek), pp. 369–375. University of California Press, Berkeley, California.
- Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science, 342, 364–366.
- Colautti RI, Manca M, Viljanen M et al. (2005) Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Molecular Ecology, 14, 1869–1879.
- Colautti RI, Maron JL, Barrett SCH (2009) Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evolutionary Applications, 3, 187–189.
- Colautti RI, Eckert CG, Barrett SCH (2010a) Evolutionary constraints on adaptive evolution during range expansion in an invasive plant. Proceedings of the Royal Society of London Series B, 277, 1799–1806.
- Colautti RI, White NA, Barrett SCH (2010b) Variation of self-incompatibility within invasive populations of purple loosestrife (Lythrum salicaria L.) from eastern North America. International Journal of Plants Sciences, 171, 158–166.
- Cox GW (2004) Alien Species and Evolution: The Evolutionary Ecology of Exotic Plants, Animals, Microbes, and Interacting Native Species. Island Press, Washington, District of Columbia.
- Crawford DJ, Vassiliki VB (2004) The Scientific Papers of G. Ledyard Stebbins (1929–2000). ARG Gantner Verlag, Ruggell, Liechtenstein.
- Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters, 14, 419–431.
- Dlugosch KLM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology, 17, 431–449.
- Dornier A, Munoz F, Cheptou P-O (2008) Allee effect and self-fertilization in hermaphrodites: reproductive assurance in a structured metapopulation. Evolution, 62, 2558–2569.
- Dybdahl MF, Kane SL (2005) Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology, 86, 1592–1601.
- Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences of the United States of America, 97, 7043–7050.
- Elton CS (1958) The Ecology of Invasions by Animals and Plants. Methuen, London.
- García-Ramos G, Rodríguez D (2002) Evolutionary speed of species invasions. Evolution, 56, 661–668.
- Golding GB, Strobeck C (1980) Linkage disequilibrium in a finite population that is partially selfing. Genetics, 94, 777–789.
- Gravuer K, Sullivan JJ, Williams PA, Duncan RP (2008) Strong human association with plant invasion success for Trifolium introductions to New Zealand. Proceedings of the National Academy of Sciences of the United States of America, 105, 6344–6349.
-
Hamrick JL, Linhart YB, Mitton JB (1979) Relationships between life history characteristics and electrophoretically detectable genetic variation in plants. Annual Review of Ecology and Systematics, 10, 173–2000.
10.1046/j.1365-2664.1999.00364.x Google Scholar
- Harris H (1966) Enzyme polymorphism in man. Proceedings of the Royal Society of London Series B, 164, 298–310.
- Higgins SI, Richardson DM (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. American Naturalist, 153, 464–475.
- Holm LG, Plucknett DL, Pancho JV, Herberger JP (1977) The World's Worst Weeds: Distribution and Biology. University of Hawaii, Press, Honolulu.
- Hulme PE (2008) Phenotypic plasticity and plant invasions: is it all Jack? Functional Ecology, 22, 3–7.
- Husband BC, Barrett SCH (1991) Colonization history and population genetic structure of Eichhornia paniculata in Jamaica. Heredity, 66, 287–296.
- Keller SR, Fields PD, Berardi Taylor DR (2014) Recent admixture generates heterozygosity-fitness correlations during the range expansion of an invading species. Journal of Evolutionary Biology, 27, 616–627.
- van Kleunen M, Johnson SD (2007) Effects of self-compatibility on the distribution range of invasive European plants in North America. Conservation Biology, 21, 1537–1544.
- van Kleunen M, Manning JC, Pasqualetto V, Johnson SD (2008) Phylogenetically independent associations between autonomous self-fertilization and plant invasiveness. American Naturalist, 171, 195–201.
- van Kleunen M, Weber E, Fischer M (2010a) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecology Letters, 13, 235–245.
- van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010b) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecology Letters, 13, 947–958.
- Kliber A, Eckert CG (2005) Interaction between founder effect and selection during biological invasion in an aquatic plant. Evolution, 59, 1900–1913.
- Konečný A, Estoup A, Duplantier J-M et al. (2013) Invasion genetics of the introduced black rat (Rattus rattus) in Senegal, West Africa. Molecular Ecology, 22, 286–3000.
- Kuester A, Conner JK, Culley T, Baucom RS (2014) How weeds emerge: a taxonomic and trait-based examination using Unites States data. New Phytologist, 202, 1055–1068.
- Lande R (1976) The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genetical Research, 26, 221–235.
- Lande R (1977) The influence of the mating system on the maintenance of genetic variability in polygenic characters. Genetics, 86, 485–498.
-
Levins R (1968) Evolution in Changing Environments. Princeton University Press, Princeton, New Jersey.
10.1515/9780691209418 Google Scholar
- Lewontin RC (1984) Detecting population differences in quantitative characters as opposed to gene frequencies. American Naturalist, 123, 115–124.
- Lewontin RC, Hubby JL (1966) A molecular approach to the study of genic heterozygosity in natural populations II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura . Genetics, 54, 595–609.
- Lynch M (1984) Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Quarterly Review of Biology, 59, 257–290.
- Martins PS, Jain SK (1979) Role of genetic variation in the colonizing ability of rose clover (Trifolium hirtum All.). American Naturalist, 114, 591–595.
- Matesanz S, Sultan SE (2013) High-performance genotypes in an introduced plant: insights into future invasiveness. Ecology, 94, 2464–2474.
- Moeller DA, Geber MA (2005) Ecological context of the evolution of self-pollination between incipient Clarkia species. Evolution, 66, 1210–1225.
- Moles AT, Gruber MA, Bonser SP (2008) A new framework for predicting invasive species. Journal of Ecology, 96, 13–17.
-
Mooney HA, Drake JA (eds) (1986) Ecology of Biological Invasions of North America. Ecological Studies 58. Springer-Verlag, New York.
10.1007/978-1-4612-4988-7 Google Scholar
- Mulligan J (2014) The Real Weed Man. Portrait of a Canadian Botanist. Gerald A. Mulligan . Privately Published. Library and Archives Canada Cataloguing in Publication, ISBN 978-0-9937698-0-1.
- Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution, 29, 1–20.
- Ness RW, Wright SI, Barrett SCH (2010) Mating-system variation, demographic history and patterns of nucleotide diversity in the tristylous plant Eichhornia paniculata . Genetics, 184, 381–392.
- Nevo E (1978) Genetic variation in natural populations: patterns and theory. Theoretical Population Biology, 13, 121–177.
- Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species. Influence of mating system and introduction dynamics. In: Species Invasions Insights into Ecology, Evolution, and Biogeography (eds DF Sax, JJ Stachowicz, DD Gaines), pp. 201–228. Sinauer & Associates, Sunderland, Massachusetts.
- Palacio-López K, Gianoli E (2011) Invasive plants do not display greater phenotypic plasticity than native or non-invasive counterparts: a meta-analysis. Oikos, 120, 1393–1401.
- Pannell JR, Barrett SCH (1998) Baker's Law revisited: reproductive assurance in a metapopulation. Evolution, 52, 657–668.
- Parker IM, Rodriguez J, Loik M (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus . Conservation Biology, 17, 59–72.
-
Parsons PA (1983) The Evolutionary Biology of Colonizing Species. Cambridge University Press, Cambridge.
10.1017/CBO9780511525742 Google Scholar
- Perrins J, Williamson M, Fitter A (1992) Do annual weeds have predictable characters? Acta Oecologica, 13, 517–533.
-
Pigliucci M (2001) Phenotypic Plasticity Beyond Nature and Nurture. John Hopkins University Press, Baltimore, Maryland.
10.56021/9780801867880 Google Scholar
- Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology, 77, 1655–1661.
- Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9, 981–993.
- Richardson DM, Pyšek P (2008) Fifty years of invasion ecology – the legacy of Charles Elton. Diversity and Distributions, 14, 161–168.
- Richardson BJ, Rogers PM, Hewitt GM (1980) Ecological genetics of the wild rabbit in Australia. II Protein variation in British, French and Australian rabbits and the geographical distribution of variation in Australia. Australian Journal of Biological Sciences, 33, 371–383.
- DF Sax, JJ Stachowicz, SD Gaines (eds) (2005) Species Invasions: Insights into Ecology, Evolution and Biogeography. Sinauer Associates, Sunderland, Massachusetts.
- Selander RK, Kaufman DW (1973) Self-fertilization and genic population structure in a colonizing land snail. Proceedings of the National Academy of Sciences of the United States of America, 70, 1186–1190.
-
Shigesada N, Kawasaki K (1997) Biological Invasions: Theory and Practice. Oxford University Press, Oxford.
10.1093/oso/9780198548522.001.0001 Google Scholar
- Simberloff D (2011) Charles Elton: neither founder nor siren. In: Fifty Years of Invasion Ecology The Legacy of Charles Elton (ed. D Richardson), pp. 11–24. Wiley-Blackwell, Oxford.
- Smocovitis VB (2001) G. Ledyard Stebbins and the evolutionary synthesis. Annual Review of Genetics, 35, 803–814.
- Smocovitis VB (2006) Keeping up with Dobzhansky: G. Ledyard Stebbins, Jr., plant evolution, and the evolutionary synthesis. History and Philosophy of the Life Sciences, 28, 9–47.
-
Stebbins GL (1950) Variation and Evolution in Plants. Columbia University Press, New York.
10.7312/steb94536 Google Scholar
- Stebbins GL (1957) Self-fertilization and population variability in the higher plants. American Naturalist, 91, 337–354.
- Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends in Ecology and Evolution, 18, 94–101.
- Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Molecular Ecology, 17, 351–360.
- Sultan SE (1987) Evolutionary implications of phenotypic plasticity in plants. Evolutionary Biology, 21, 127–178.
- Sultan SE, Horgan-Kobelski T, Nichols LM, Riggs C, Waples RK (2012) A resurrection study reveals rapid adaptive evolution within populations of an invasive plant. Evolutionary Applications, 6, 266–278.
- Therriault TW, Orlova MI, Docker MF, MacIsaac HJ, Heath DD (2005) Invasion genetics of a freshwater mussel (Dreissena rostriformis bugensis) in eastern Europe: high gene flow and multiple introductions. Heredity, 95, 16–23.
- Villablanca FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Molecular Ecology, 7, 547–560.
- Westley PAH (2011) What invasive species reveal about the rate and form of contemporary phenotypic change in nature. American Naturalist, 177, 496–509.
- Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14, 569–580.
- Williamson M (1996) Biological Invasions. Chapman and Hall, London.
- Williamson MH, Fitter A (1996) The characters of successful invaders. Biological Conservation, 78, 163–170.
- Zhan A, MacIsaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Molecular Ecology, 19, 4678–4694.
- Zhang Y-Y, Zhang D-Y, Barrett SCH (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Molecular Ecology, 19, 1774–1786.