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The evolution of invasive ability Sébastien Lavergne University of Vermont, Dept. of Botany What is an invasive species ? • A species that invades an habitat where it previously did not exist before and grows without limit causing changes in the community and ecosystem • Invasive Species vs. Alien Species Alien species = a non-native species Invasive species = alien species that harms communities and ecosystems • Four stages necessary for a successful invasion : 1. 2. 3. 4. Dispersal/transport to a new range Initial colonization Establishment (and lag phase) Secondary spread • Consequences of invasive species Alter community composition and structure Alter ecosystem structure, processes and function Disease transmission Large economic costs What makes a species invasive when translated into a new region ? Sakai et al. (2001) Ann. Rev. Ecol. Syst. 32: 305-332 Lloret et al. (2005) J. of Ecology 93: 512-520 • Characteristics of the recipient community - disturbance frequency - resource availability and fluctuation - species / functional diversity • Traits of invasive species - sexual and asexual reproduction rapid growth, and short time to maturity long flowering / emergence period good dispersal ability good competitive ability / large size … but recipient communities and alien species are not fixed entities… Why studying evolution in invasive species ? • Introduced species recently experienced a new environment, and therefore new selective pressure. -> A live experiment of natural selection John N. Thompson 1998. Rapid evolution as an ecological process. Trends in Ecology & Evolution, 13:8:329-332 Rapid evolution of interspecific interactions (during a time span of about 100 years) has the potential to be an important influence on the ecological dynamics of communities. However, despite the growing number of examples, rapid evolution is still not a standard working hypothesis for many ecological studies on the dynamics of population structure or the organization of communities. Analysis of rapid evolution as an ecological process has the potential to make evolutionary ecology one of the most central of applied biological sciences. • Genetics processes likely to influence invasive species dynamics… - genetic bottlenecks / genetic drift - natural selection - recombination / hybridization Consequences of genetic bottlenecks on introduced populations • Loss of genetic diversity native range introduction Binomial sampling (N, pt) linked to the dispersal / establishment phase • Linkage (gametic) disequilibrium native range 2 genes, 2 alleles per genes = 4 possible types of gamete introduction during a bottleneck, some combinations might be lost and statistical association between alleles created Bottlenecks in introduced ant populations Tsutsui et al. (2000) Proc. Natl. Acad. Sci. USA 97: 5948-5953 Invasion of Argentine ants in California Linepithema humile Genetic diversity Aggressive behavior with conspecifics Introduced (California) Native (Argentina) H=0.204 H=0.639 no yes Bottlenecks in introduced plant populations Eckert et al. (1996) Evolution 50(4): 1512-1519 Invasion of Lythrum salicaria (purple loosestrife) L (ssmm) S M (S---) (ssM-) • Mating is not possible between two individuals of the same type (incompatibility within morphs => disassortative mating between morphs) • The potential number of mates for one type in a population decreases with its frequency (negative frequency dependence) Bottlenecks in introduced plant populations continued Eckert et al. (1996) Evolution 50(4): 1512-1519 Invasion of Lythrum salicaria (purple loosestrife) Morph loss in ~5% of populations in France vs. 23% in Ontario Bottlenecks are not the rule of invasions Kolbe et al. (2004) Nature 431: 177-181 Invasion of a Cuban lizard Brown anole (Anolis sagrei) Evolution of Increased Competitive Ability EICA hypothesis Blossey & Nötzold (1995) Journal of Ecology 83:887-889 Release from enemies allows selection from higher growth selection native range growth introduced range - - defense transport no enemies natural enemies Evolution of Increased Competitive Ability continued Siemann & Rogers (2001) Ecology Letters 4:514-518 Invasion of Sapium setiferum (Chinese tallow tree) Enemy release but no EICA Genton et al. (2005) Oecologia 146:404-414 Invasion of Ambrosia artemisiifolia (common ragweed) Novel weapons hypothesis Another mechanism of EICA Callaway & Aschebourg (2000) Science 290:521-523 Allelopathic effects on neighbors are stronger in the introduced range introduced range native range naive community - - co-adapted community - transport - - Novel weapons hypothesis continued Callaway & Aschebourg (2000) Science 290:521-523 Invasion of Centaurea maculosa (spotted knapweed) Bais et al. (2003) Science 301:1377-1380 Evolutionary increase in reproductive vigor Brown & Eckert 2005. American Journal of Botany 92(3):495-502 Invasion of Butomus umbellatus (flowering rush) Hybridization and evolution of invasiveness Ellstrand & Schierenbeck (2000) Proc. Natl. Acad. Sci. USA 97(13):7043-7050 • Literature review : 28 well supported examples of invasive species that are hybridized and which parent species are not invasive • How inter-specific hybridization may catalyze the evolution of invasive ability : Species A Species B F1 segregation recombination translocation recombination translocation chromosome doubling * * Increased variation Evolutionary Purge of novelty genetic load Fixed heterosis Hybridization and evolution of invasiveness continued Gaskin et al. (2002) Proc. Natl. Acad. Sci. USA 99:11256-11259 Invasion of Tamarix spp. Evolution of resistance to invasive species? Callaway et al. (2005) Journal of Ecology 93:576-583 Tolerance of native American plant species to allelo-chemicals of Centaurea maculosa The evolution of invasive ability Conclusions • Invasiveness may be a trait that has evolved after establishment of alien species rather than a pre-adaptation -> limited power of predictive approaches from species traits in their native range • Template for evolution of invasive ability: - bottlenecks and creation of new genetic structure in populations - multiple introductions that increase local genetic diversity - recombination between genetically distinct genotypes (or hybridization between distinct species) can create novel genotypes