Abstract
The role of preadaptation in ecology and evolution is determined by how the traits evolved by a species in one environment allow it to be successful in novel environments. This concept bears directly on modern biological invasions, as species are introduced to new locations beyond their historical borders. In this study, we used a phylogenetically-controlled analysis of the flowering plant genus Silene (Caryophyllaceae) to show that native geographic range size, along with a suite of life history traits affecting plant growth and reproduction, have preadapted some species for the invasion of new ranges. Using a path analytic approach, we further show that some of the covariance between life history traits and invasiveness is indirect, caused by mutual associations with native range size. Specifically, we found that reproductive traits such as the number of flowers per inflorescence and length of the flowering season directly preadapt species for invasion, while plant height is indirectly associated with invasion through a correlation with native range size. Other traits such as ovule number and leaf size are both directly and indirectly associated with invasion success. Our results reveal the importance of accounting for correlations among plant traits and geographic range size when predicting preadaptation for invasiveness. We also highlight that the traits predictive of invasion success among species of Silene are often those found to be rapidly evolving within introduced populations, suggesting common forces of selection operating at these different biological scales of organization during invasion.
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References
Antonovics J (1976) The input from population genetics: “the new ecological genetics”. Syst Bot 1:233–245
Andersson S, Mansby E, Prentice HC (2008) Paternal effects on seed germination: a barrier to the genetic assimilation of an endemic plant taxon? J Evol Biol 21:1408–1417
Baker HG (1948) Stages in invasion and replacement demonstrated by species of Melandrium. J Ecol 36:96–119
Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–348
Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24
Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16
Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF, Filatov D, Giraud T, Hood ME, Marais GAB, McCauley D, Pannell JR, Shykoff JA, Vyskot B, Wolfe LM, Widmer A (2009) Silene as a model system in ecology and evolution. Heredity 103:5–14
Bininda-Emonds ORP (2004) The evolution of supertrees. Trends Ecol Evol 19:315–322
Blackburn TH, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197
Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042
Blomberg SP, Garland T, Ives AR, Crespi B (2009) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Blossey B, Notzold R (1995) Evolution of inceased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889
Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279
Brown JH, Stevens GC, Kaufman DM (1996) The geographic range: size, shape, boundaries, and internal structure. Annu Rev Ecol Syst 27:597–623
Burns JH (2006) Relatedness and environment affect traits associated with invasive and noninvasive introduced Commelinaceae. Ecol Appl 16:1367–1376
Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488
Desfeux C, Maurice S, Henry JP, Lejeune B, Gouyon PH (1996) Evolution of reproductive systems in the genus Silene. Proc R Soc B Biol Sci 263:409–414
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Frajman B, Eggens F, Oxelman B (2009) Hybrid origins and homoploid reticulate evolution within heliosperma (sileneae, caryophyllaceae)–a multigene phylogenetic approach with relative dating. Syst Bot 58:328–345
Frappier B, Eckert RT (2003) Utilizing the USDA PLANTS database to predict exotic woody plant invasiveness in New Hampshire. For Ecol Manag 185:207–215
Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer Associates, Sunderland, MA
Gleason HA, Cronquist A (1991) Manual of vascular plants of Northeastern United States and adjacent Canada. The New York Botanical Garden, Bronx, New York
Goodwin BJ, McAllister AJ, Fahrig L (1999) Predicting invasiveness of plant species based on biological information. Conserv Biol 13:422–426
Gould SJ, Vrba ES (1982) Exaptation–a missing term in the science of form. Paleobiology 8:4–15
Greuter W (1995) Silene (Caryophyllaceae) in Greece—a subgeneric and sectional classification. Taxon 44:543–581
Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford, VIII, p 235
Hayes K, Barry S (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506
Hitchcock CL, Maguire B (1947) A revision of the North American species of Silene. Univ Wash Publ Biol 13:1–73
Holt RD (2003) On the evolutionary ecology of species’ ranges. Evol Ecol Res 5:159–178
Hood ME, Mena-Alí JI, Gibson AK, Oxelman B, Giraud T, Yockteng R, Arroyo MTK, Conti F, Pedersen AB, Gladieux P, Antonovics J (2010) Distribution of the anther-smut pathogen Microbotryum on species of the Caryophyllaceae. New Phytologist 187:217–229
Jalas J, Suominen J (1986) Atlas Florae Europaeae, vol 3. Cambridge University Press, Cambridge, UK
Johnson MTJ, Smith SD, Rausher MD (2010) Effects of plant sex on range distributions and allocation to reproduction. New Phytol 186:769–779
Jurgens A, Witt T, Gottsberger G (2002) Pollen grain numbers, ovule numbers and pollen-ovule ratios in Caryophylloideae: correlation with breeding system, pollination, life form, style number, and sexual system. Sex Plant Reprod 14:279–289
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Keller SR, Taylor DR (2008) History, chance, and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866
Keller M, Kollmann J, Edwards PJ (2000) Genetic introgression from distant provenances reduces fitness in local weed populations. J Appl Ecol 37:647–659
Keller SR, Sowell DR, Neiman M, Wolfe LM, Taylor DR (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytologist 183:678–690
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytol 169:667–680
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: epidemiology, global consequences, and control. Ecol Appl 10:689–710
Martindale IC (1876) The introduction of foreign plants. Botanical Gazette 2:55–58
McNeill J (1977) The biology of Canadian weeds. 25. Silene alba (Miller) EHL Krause. Can J Plant Sci 57:1103–1114
Muth NZ, Pigliucci M (2006) Traits of invasives reconsidered: phenotypic comparisons of introduced invasive and introduced noninvasive plant species within two closely related clades. Am J Bot 93:188–196
Oxelman B, Liden M (1995) Generic boundaries in the tribe sileneae (Caryophyllaceae) as inferred from Nuclear Rdna sequences. Taxon 44:525–542
Oxelman B, Liden M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst Evol 206:393–410
Oxelman B, Liden M, Rabeler RK, Popp M (2000) A revised generic classification of the tribe Sileneae (Caryophyllaceae). Nord J Bot 20:743–748
Peterson AT, Soberon J, Sanchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267
Pettersson MW (1991) Pollination by a guild of fluctuating moth populations: option for unspecialization in silene vulgaris. J Ecol 79:591–604
Popp M, Oxelman B (2004) Evolution of a RNA polymerase gene family in Silene (Caryophyllaceae)—incomplete concerted evolution and topological congruence among paralogues. Syst Biol 53:914–932
Prentice HC, Malm JU, Hathaway L (2008) Chloroplast DNA variation in the European herb Silene dioica (red campion): postglacial migration and interspecific introgression. Plant Syst Evol 272:23–37
Prinzing A, Durka W, Klotz S, Brandl R (2001a) Which species become aliens? Evol Ecol Res 4:385–405
Prinzing A, Durka W, Klotz S, Brandl R (2001b) The niche of higher plants: evidence for phylogenetic conservatism. Proc R Soc Lond B Biol Sci 268:2383–2389
Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analyzing comparative data. CABIOS 11:247–251
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? Biol Invasions 193:97–125
Pysek P, Jarosík V, Pergl J, Randall R, Chytrý M, Kühn I, Tichý L, Danihelka J, Chrtek Jun J, Sádlo J (2009) The global invasion success of Central European plants is related to distribution characteristics in their native range and species traits. Divers Distrib 15:891–903
Rabeler RK, Hartman RL (2005) Silene. In: Flora of North America Editorial Committee e (ed) Flora of North America North of Mexico. New York and Oxford, pp 3–215
Randall RP (2002) A global compendium of weeds. R.G and F.J. Richardson, Melbourne, p 906
Randle AM, Slyder JB, Kalisz S (2009) Can differences in autonomous selfing ability explain differences in range size among sister-taxa pairs of Collinsia (Plantaginaceae)? An extension of Baker’s Law. New Phytol 183:618–629
Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Ricklefs RE, Latham RE (1992) Intercontinental correlation of geographical ranges suggests stasis in ecological traits of relict genera of temperate perennial herbs. Am Nat 139:1305–1321
Ricklefs RE, Guo QF, Qian H (2008) Growth form and distribution of introduced plants in their native and non-native ranges in Eastern Asia and North America. Divers Distrib 14:381–386
Runyeon-Lager H, Prentice HC (2000) Morphometric variation in a hybrid zone between the weed, Silene vulgaris, and the endemic, Silene uniflora ssp petraea (Caryophyllaceae), on the Baltic island of Oland. Can J Bot Rev Can Bot 78:1384–1397
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Salamin N, Hodkinson TR, Savolainen V (2002) Building supertrees: an empirical assessment using the grass family (Poaceae). Syst Biol 51:136–150
Sanderson MJ, Purvis A, Henze C (1998) Phylogenetic supertrees: assembling the trees of life. Trends Ecol Evol 13:105–109
SAS (2004) SAS 9.1.3. Cary, NC
Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101
Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360
Sutherland S (2004) What makes a weed a weed: life history traits of native and exotic plants in the USA. Oecologia 141:24–39
Svenning J-C, Skov F (2007) Could the tree diversity pattern in Europe be generated by postglacial dispersal limitation? Ecol Lett 10:453–460
Swofford D (1998) Phylogenetic analysis using parsimony (and other methods) PAUP* 4.04b. Sinauer Associates, Sunderland, MA
Taylor DR, Keller SR (2007) Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61:334–345
Thebaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236
Trigas P, Iatrou G, Karetsos G (2007) Species diversity, endemism and conservation of the family Caryophyllaceae in Greece. Biodivers Conserv 16:357–376
van Kleunen M, Manning JC, Pasqualetto V, Johnson SD (2008) Phylogenetically independent associations between autonomous self-fertilization and plant invasiveness. Am Nat 171:195–201
Webb JK, Brown GP, Child T, Greenlees MJ, Phillips BL, Shine R (2008) A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid toxic cane toads. Austral Ecol 33:821–829
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2003) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159
Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580
Wiens JJ, Graham CH (2005) Niche conservatism: Integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539
Williamson MH (1996) Biological invasions. Chapman and Hall, London
Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170
Wolfe LM (2002) Why alien invaders succeed: support for the escape from enemies hypothesis. Am Nat 160:705–711
Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7:813–820
Zar J (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ
Acknowledgments
We thank D. Taylor for guidance and research support, J. Antonovics, M. Neiman, and the Taylor lab group for helpful discussion, B. Oxelman for kindly reviewing the phylogenetic relationships in our supertree, and J. Mena-Ali for sharing data on Microbotryum infection. M. Cadotte and 2 anonymous reviewers provided comments that greatly improved the manuscript. This work was supported by NSF-DEB 0608358.
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Jenkins, C., Keller, S.R. A phylogenetic comparative study of preadaptation for invasiveness in the genus Silene (Caryophyllaceae). Biol Invasions 13, 1471–1486 (2011). https://doi.org/10.1007/s10530-010-9907-4
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DOI: https://doi.org/10.1007/s10530-010-9907-4