Abstract
Spread of smooth cordgrass (Spartina alterniflora) in China is an exceptional example of unanticipated outcomes arising from intentional introductions. It has been proposed that in China, management strategies used to establish S. alterniflora inadvertently promoted evolutionary outcomes that have contributed to other Spartina invasions. In this study, we assessed whether S. alterniflora in China exhibits genetic signatures of mechanisms known to promote invasion success, including large founding populations, evolved self-fertility, ‘superior source ecotypes’, and post-introduction admixture. This involved comparing microsatellite genotype and chloroplast haplotype variation among Chinese populations to other invasive S. alterniflora populations as well as native range populations, inclusive of samples from all reported source areas. We found distinct signatures of source population contributions to Chinese populations, as well as evidence of post-introduction admixture, and no evidence of limitations from a genetic bottleneck. Measures of inbreeding were well below what has been found in other non-native populations that have evolved self-fertility. Differences in genetic diversity among sites were similar to latitudinal patterns in the native range, but could be attributable to introduction history. Comparisons to other invasive populations indicate that a combination of common and idiosyncratic processes have contributed to the success of S. alterniflora in China and elsewhere, with intentional introductions promoting mechanisms that accelerate rates of spread and widespread invasion.
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References
Adams JB, Grobler A, Rowe C et al (2012) Plant traits and spread of the invasive salt marsh grass, Spartina alterniflora Loisel., in the Great Brak Estuary, South Africa. Afr J Mar Sci 34:313–322
Ainouche ML, Fortune PM, Salmon A et al (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173
An SQ, Gu BH, Zhou CF et al (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res 47:183–191
An SQ, Wang ZS, Zhou CF (2010) Varying success of Spartina spp. invasions in China: genetic diversity or differentiation? In: Ayres DR, Kerr DW, Ericson SD, Olofson PR (eds) Proceedings of the third international conference on invasive Spartina, 2004 Nov 8–10, San Francisco, CA, USA. San Francisco Estuary Invasive Spartina Project of the California State Coastal Conservancy, Oakland, pp 33–36
Ayres DR, Grotkopp E, Zaremba K et al (2008) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95:713–719
Blum MJ, Sloop CM, Ayres DR, Strong DR (2004) Characterization of microsatellite loci in Spartina species (Poaceae). Mol Ecol Notes 4:39–42
Blum MJ, Bando KJ, Katz M, Strong DR (2007) Geographic structure, genetic diversity and source tracking of Spartina alterniflora. J Biogeogr 34:2055–2069
Castillo JM, Ayres DR, Leira-Doce P et al (2010) The production of hybrids with high ecological amplitude between exotic Spartina densiflora and native S. maritima in the Iberian Peninsula. Divers Distrib 16:547–558
Chen JQ, Chung CH (1990) Genecological studies of Spartina alterniflora. In: Wang Y (ed) Proceedings of the fifth MICE symposium for Asia and the Pacific. Nanjing University Press, Nanjing, pp 168–183
Chung CH (1993) Thirty years of ecological engineering with Spartina plantations in China. Ecol Eng 2:261–289
Chung CH (2004) Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecol Eng 23:135–150
Chung CH (2006) Forty years of ecological engineering with Spartina plantations in China. Ecol Eng 27:49–57
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846
Daehler CC (1998) Variation in self-fertility and the reproductive advantage of self-fertility for an invading plant (Spartina alterniflora). Evol Ecol 12:553–568
Daehler CC, Anttila CK, Ayres DR et al (1999) Evolution of a new ecotype of Spartina alterniflora (Poaceae) in San Francisco Bay, California, USA. Am J Bot 86:543–546
Deng Z, An S, Zhou C et al (2007) Genetic structure and habitat selection of the tall form Spartina alterniflora Loisel. in China. Hydrobiologia 583:195–204
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449
Eppinga MB, Rietkerk M, Dekker SC et al (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Ewel JJ, O’Dowd DJ, Bergelson J et al (1999) Deliberate introductions of species: research needs—benefits can be reaped, but risks are high. Bioscience 49:619–630
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Gagne RB, Hogan JD, Pracheil BM et al (2015) Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host. Freshw Biol 60:311–322
Hengeveld R (1989) Dynamics of biological invasions. Chapman and Hall, New York
Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15
Hovick SM, Whitney KD (2014) Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis. Ecol Lett 17:1464–1477
Jiang FX, Lu BS (1985) Biological characteristics of three American species of Spartina and the nutrient analysis. J Nanjing Univ (Special issue for research advances in Spartina: achievements of past 22 years):302–309
Li B, Liao C, Zhang X et al (2009) Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol Eng 35:511–520
Liu W, Maung-Douglass K, Strong DR et al (2016) Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China. J Ecol 104:173–181
Mack RN, Erneberg M (2002) The United States naturalized flora: largely the product of deliberate introductions. Ann Mo Bot Gard 89:176–189
Marchant CJ (1968) Evolution in Spartina (Gramineae): III. Species chromosome numbers and their taxonomic significance. J Linn Soc Lond Bot 60:411–417
Martin PH, Canham CD, Marks PL (2008) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149
McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21:297–302
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genet 67:170–181
Qin P, Jing MD, Xie M (1985) The comparison of community biomass among the three ecotypes of Spartina alterniflora on the beach of estuary Luoyuan Bay, Fujian. J Nanjing Univ (Special issue for research advances in Spartina: achievements of past 22 years):226–236
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464
Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20
Sloop CM, McGray HG, Blum MJ, Strong DR (2005) Characterization of 24 additional microsatellite loci in Spartina species (Poaceae). Conserv Genet 6:1049–1052
Sloop CM, Ayres DR, Strong DR (2009) The rapid evolution of self-fertility in Spartina hybrids (Spartina alterniflora × foliosa) invading San Francisco Bay, CA. Biol Invasions 11:1131–1144
Sprehn CG, Blum MJ, Quinn TP, Heins DC (2015) Landscape genetics of Schistocephalus solidus parasites in threespine stickleback (Gasterosteus aculeatus) from Alaska. PLoS One 10:e0122307
Strong DR, Ayres DA (2009) Spartina introductions and consequences in salt marshes: arrive, survive, thrive, and sometimes hybridize. In: Silliman BR, Bertness MD, Grosholz ED (eds) Human impacts on salt marshes: a global perspective. University of California Press, Berkeley, pp 3–22
Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annu Rev Ecol Evol Syst 44:389–410
Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Travis SE, Proffitt CE, Lowenfeld RC, Mitchell TW (2002) A comparative assessment of genetic diversity among differently-aged populations of Spartina alterniflora on restored versus natural wetlands. Restor Ecol 10:37–42
Wang XY, Shen DW, Jiao J et al (2012) Genotypic diversity enhances invasive ability of Spartina alterniflora. Mol Ecol 21:2542–2551
Xia L, Zhao H, Yang W, An S (2014) Genetic diversity, ecotype hybrid, and mixture of invasive Spartina alterniflora Loisel in Coastal China. CLEAN Soil Air Water. doi:10.1002/clen.201300882
Xu GW, Zhuo RZ (1985) Preliminary studies of introduced Spartina alterniflora Loisel in China. J Nanjing Univ (Special edition for research advances in Spartina: achievements of past 22 years):212–225
Zhang RS, Shen YM, Lu LY et al (2004) Formation of Spartina alterniflora salt marshes on the coast of Jiangsu Province, China. Ecol Eng 23:95–105
Zhi Y, Li H, An S et al (2007) Inter-specific competition: Spartina alterniflora is replacing Spartina anglica in coastal China. Estuar Coast Shelf Sci 74:437–448
Zuo P, Zhao SH, Liu CA et al (2012) Distribution of Spartina spp. along China’s coast. Ecol Eng 40:160–166
Acknowledgments
We would like to thank J. Derek Hogan and Ryan Walter for assisting with laboratory analyses. We are also grateful for the logistical support provided from Jianjian Lu, Shieh tsing Hsieh, John McLachlan, Douglas Meffert, and Torbjörn Törnqvist through the Tulane University-East China Normal University Ecopartnership. Funding for this work was made available from East China Normal University and the Tulane-Xavier Center for Bioenvironmental Research, Science and Technology Innovation Project of Colleges and Universities in Guangdong Province (No. 2012KJCX0080) and Researching Fund for Professors and Doctors, Guangdong University of Education (No. 11ARF02).
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Brittany M. Bernik and Haisheng Li have contributed equally to this paper.
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Bernik, B.M., Li, H. & Blum, M.J. Genetic variation of Spartina alterniflora intentionally introduced to China. Biol Invasions 18, 1485–1498 (2016). https://doi.org/10.1007/s10530-016-1096-3
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DOI: https://doi.org/10.1007/s10530-016-1096-3