Abstract
Gypsophila paniculata (baby’s breath) is a popular garden ornamental and horticultural crop introduced to North America in the late 1800s. After introduction it quickly spread, often forming dense monotypic stands and crowding out native species. To better understand this invasion, samples of G. paniculata from seven distinct populations spanning a portion of the plant’s invaded range within the United States (Washington, North Dakota, Minnesota, and Michigan) were collected and genotyped using 14 microsatellite loci. Population structure was inferred using both Bayesian and multivariate methods. The results suggest the presence of at least two genetic clusters among the seven sampling locations, with samples from Washington, North Dakota, Minnesota, and northwestern Michigan forming one genetic cluster and the second cluster consisting of two more southern sampling locations in Michigan. Public herbarium records were used to examine the invasion status (expansion vs. plateau phase) of the identified genetic clusters for G. paniculata. Invasion curves were created from a database of 351 herbarium collections dating from the late 1800s to current day. Results showed that time periods of invasion differed between the two genetics clusters, suggesting at least two invasion events. Patterns of reduced genetic diversity within the earlier invasion could reflect limited standing genetic variation during the initial period of this horticultural species’ import. This study emphasizes how anthropogenic influences can shape the study of invasive plant ecology, particularly when considering species popular in the botanical or horticultural industries.
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References
Abdelkrim J, Pascal M, Calmet C, Samadi S (2005) Importance of assessing population genetic structure before eradication on invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518
Ahroni A, Zuker A, Rozen Y, Shejtman H, Vainstein A (1997) An efficient method for adventitious shoot regeneration from stem-segment explants of Gypsophila. Plant Cell Tiss Org 49(2):101–106
Aikio S, Duncan RP, Hulme PE (2010) Lag-phases in alien plant invasions: separating the facts from the artefacts. Oikos 119:370–378. https://doi.org/10.1111/j.1600-0706.2009.17963.x
Antunes PM, Schamp B (2017) Constructing standard invasion curves from herbarium data—toward increased predictability of plant invasions. Invasive Plant Sci Manag 10:293–303. https://doi.org/10.1017/inp.2017.38
Archer FI, Adams PE, Schneiders BB (2016) stratag: an R package for manipulation, summarizing and analysing population genetic data. Mol Ecol Resour 17:5–11. https://doi.org/10.1111/1755-0998.12559
Barkoudah YI (1962) A revision of Gypsophila, Bolathus, Ankyropetalum and Phryna. Wentia 9:1–203. https://doi.org/10.1111/j.1438-8677.1962.tb00012
Baskett CA, Emery SM, Rudgers JA (2011) Pollinator visits to threatened species are restored following invasive plant removal. Int J Plant Sci 172:411–422. https://doi.org/10.1086/658182
Boag AE, Eckert CG (2013) The effect of host abundance on the distribution and impact of biocontrol agents on purple loosestrife (Lythrum salicaria, Lythraceae). Écoscience 20:90–99. https://doi.org/10.2980/20-1-3549
Brzuszek RF, Harkess RL (2009) Green industry survey of native plant marketing in the southeastern United States. Horttechnology 19:168–172. https://doi.org/10.21273/hortsci.19.1.168
Crooks JA (2007) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Écoscience 12:316–329. https://doi.org/10.2980/i1195-6860-12-3-316.1
Darwent AL (1975) The biology of Canadian weeds: 14. Gypsophila paniculata L. Biol Can Weeds 55:1049–1058. https://doi.org/10.4141/cjps75-164
Darwent AL, Coupland RT (1966) Life history of Gypsophila paniculata. Weeds 14:313. https://doi.org/10.2307/4040974
Darwent AL, Coupland RT, Skoglund NA (1967) The potential of Gypsophila paniculata as a weed in Saskatchewan. Can J Plant Sci 47:125–134. https://doi.org/10.4141/cjps67-022
Dehnen-Schmutz K, Touza J, Perrings C, Williamson M (2007) A century of the ornamental plant trade and its impact on invasion success. Divers Distrib 13:527–534. https://doi.org/10.1111/j.1472-4642.2007.00359.x
Dullinger I, Wessely J, Bossdorf O et al (2017) Climate change will increase the naturalization risk from garden plants in Europe. Glob Ecol Biogeogr 26:43–53. https://doi.org/10.1111/geb.12512
Dupuis JR, Janes JK, Malenfant RM et al (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602. https://doi.org/10.1111/mec.14187
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
EDDMapS (2019) Early detection & distribution mapping system. The University of Georgia-Center for Invasive Species and Ecosystem Health. https://www.eddmaps.org/. https://www.eddmaps.org/distribution/usstate.cfm?sub=5682. Accessed 25 Feb 2019
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Evol Sys 24:217–242. https://doi.org/10.1146/annurev.es.24.110193.001245
Emery SM, Doran PJ (2013) Presence and management of the invasive plant Gypsophila paniculata (baby’s breath) on sand dunes alters arthropod abundance and community structure. Biol Conserv 161:174–181. https://doi.org/10.1016/j.biocon.2013.03.015
Emery SM, Doran PJ, Legge JT, Kleitch M, Howard S (2013) Aboveground and belowground impacts following removal of the invasive species baby’s breath (Gypsophila paniculata) on lake michigan sand dunes: plant and soil impacts of G. paniculata removal. Restor Ecol 21:506–514. https://doi.org/10.1111/j.1526-100X.2012.00915.x
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fuentes N, Ugarte E, Kühn I, Klotz S (2008) Alien plants in Chile: inferring invasion periods from herbarium records. Biol Invasions 10:649–657. https://doi.org/10.1007/s10530-007-9159-0
Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
Guo WY, van Kleunen M, Pierce S et al (2019) Domestic gardens play a dominant role in selecting alien species with adaptive strategies that facilitate naturalization. Glob Ecol Biogeogr 28:628–639. https://doi.org/10.1111/geb.12882
Haeuser E, Dawson W, van Kleunen M (2019) Introduced garden plants are strong competitors of native and alien residents under simulated climate change. J Ecol 107:1328–1342. https://doi.org/10.1111/1365-2745.13101
Harris C, Jiang H, Liu D et al (2009) Testing the roles of species native origin and family membership in intentional plant introductions using nursery data across the state of Kentucky. J Torrey Bot Soc 136:122–127. https://doi.org/10.3159/08-ra-080r1.1
Haynes GD, Gilligan DM, Grewe P, Nicholas FW (2009) Population genetics and management units of invasive common carp Cyprinus carpio in the Murray-Darling Basin, Australia. J Fish Biol 75:295–320. https://doi.org/10.1111/j.1095-8649.2009.02276.x
Herrero R, Asins MJ, Carbonell EA, Navarro L (1996) Genetic diversity in the orange subfamily Aurantioideae. I. Intraspecies and intragenus genetic variability. Theor Appl Genet 92:599–609
Horvitz N, Wang R, Wan FH, Nathan R (2017) Pervasive human-mediated large-scale invasion: analysis of spread patterns and their underlying mechanisms in 17 of China’s worst invasive plants. J Ecol 105:85–94. https://doi.org/10.1111/1365-2745.12692
Hulme PE (2012) Weed risk assessment: a way forward or a waste of time? J Appl Ecol 49:10–19. https://doi.org/10.1111/j.1365-2664.2011.02069.x
Hulme PE, Brundu G, Carboni M et al (2018) Integrating invasive species policies across ornamental horticulture supply chains to prevent plant invasions. J Appl Ecol 55:92–98. https://doi.org/10.1111/1365-2664.12953
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Karamanski TJ (2000) A nationalized lakeshore: the creation and administration of Sleeping Bear Dunes National Lakeshore. US Government Publishing Office, Washington, DC, USA
Kelager A, Pedersen JS, Bruun HH (2013) Multiple introductions and no loss of genetic diversity: invasion history of Japanese Rose, Rosa rugosa, in Europe. Biol Invasions 15:1125–1141. https://doi.org/10.1007/s10530-012-0356-0
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. https://doi.org/10.1016/S0169-5347(02)02489-8
Kleist A, Herrera-Reddy AM, Sforza R, Jasieniuk M (2014) Inferring the complex origins of horticultural invasives: French broom in California. Biol Invasions 16:887–901. https://doi.org/10.1007/s10530-013-0546-4
Kowarik I (1995) Time lags in biological invasions with regard to the success and failure of alien species. In: Plant invasions: general aspects and special problems. Workshop held at Kostelec nad Černými lesy, Czech Republic, 16–19 September 1993, pp 15–38
Kowarik I (2003) Human agency in biological invasions: secondary releases foster naturalization and population expansion of alien plant species. Biol Invasions 5:293–312. https://doi.org/10.1023/b:binv.0000005574.15074.66
Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838. https://doi.org/10.1007/s10530-011-0119-3
Lavoie C, Jodoin Y, De Merlis AG (2007) How did common ragweed (Ambrosia artemisiifolia L.) spread in Quebec? a historical analysis using herbarium records. J Biogeogr 34:1751–1761. https://doi.org/10.1111/j.1365-2699.2007.01730.x
Leimbach-Maus HB, Parks SR, Partridge CG (2018) Microsatellite primer development for the invasive perennial herb Gypsophila paniculata (Caryophyllaceae). Appl Plant Sci 6:e1203. https://doi.org/10.1002/aps3.1203
Leimbach-Maus HB, McCluskey EM, Locher A, Parks SR, Partridge CG (2020) Genetic structure of invasive baby’s breath (Gypsophila paniculata) populations in a Michigan dune system. Plants 9:1123. https://doi.org/10.3390/plants9091123
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. https://doi.org/10.1016/j.tree.2005.02.004
Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Meimberg H, Milan NF, Karatassiou M et al (2010) Patterns of introduction and adaptation during the invasion of Aegilops triuncialis (Poaceae) into Californian serpentine soils. Mol Ecol 19:5308–5319. https://doi.org/10.1111/j.1365-294X.2010.04875.x
Michigan Department of Natural Resources (DNR) (2014) Michigan invasive species grant program handbook, p 26, https://www.michigan.gov/documents/dnr/2014-MISGP-handbook_486956_7.pdf. Accessed 2018-03-05
Peakall R, Smouse PE (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
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. https://doi.org/10.1093/bioinformatics/bts460
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic cost associated with alien-invasive species in the United States. Ecol Econ 52:273–288. https://doi.org/10.1016/j.ecolecon.2004.10.002
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus data. Genetics 155:945–959
Pyšek P, Jarošík V, Müllerová J et al (2008) Comparing the rate of invasion by Heracleum mantegazzianum at continental, regional, and local scales. Divers Distrib 14:355–363. https://doi.org/10.1111/j.1472-4642.2007.00431.x
R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/
Rady MR (2006) In vitro culture of Gypsophila paniculata L. and random amplified polymorphic DNA analysis of the propagated plants. Biol Plant 50:507–513. https://doi.org/10.1007/s10535-006-0080-7
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution (N Y) 49:1280–1283. https://doi.org/10.2307/2410454
Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103–113. https://doi.org/10.1641/0006-3568(2001)051[0103:haapoi]2.0.co;2
Reid ML, Emery SM (2018) Scale-dependent effects of Gypsophila paniculata invasion and management on plant and soil nematode community diversity and heterogeneity. Biol Conserv 224:153–161. https://doi.org/10.1016/j.biocon.2018.05.026
Reinhold CG (1856) The farmer’s promotion book. W.S. Haven, Pittsburgh
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037
Stevens OA (1957) Weights of seeds and numbers per plant. Weeds 5:46–55. https://doi.org/10.2307/4040327
Swearingen J, Bargeron C (2016) Invasive plant atlas of the United States. University of Georgia Center for Invasive Species and Ecosystem Health. invasiveplantatlas.org. Accessed 17 Mar 2019
Van Der Veken S, Hermy M, Vellend M et al (2008) Garden plants get a head start on climate change. Front Ecol Environ 6:212–216. https://doi.org/10.1890/070063
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vettori L, Schiff S, Tani C, Pasqualetto P, Bennici A (2015) Morphological and cytological observations of wild species and hybrids of Gypsophila. Plant Biosyst 149(2):322–328
Weir BS, Cockerham CC (1983) Estimating F-statistics for the analysis of population structure. Evolution (N Y) 38:1358. https://doi.org/10.2307/2408641
Wilcove DS, Rothstein D, Dubow J et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11(10):413–418
Zalewski A, Michalska-Parda A, Bartoszewicz M et al (2010) Multiple introductions determine the genetic structure of an invasive species population: American mink Neovison vison in Poland. Biol Conserv 143:1355–1363. https://doi.org/10.1016/j.biocon.2010.03.009
Acknowledgements
The authors would like to thank Hailee Leimbach-Maus and Emma Rice for their help in the field, Kurt Thompson for his assistance mapping herbarium samples, Dr. Kathryn Turner for her comments on this manuscript, and two anonymous reviewers for their feedback during the review process. Additionally, the authors would like to thank the Environmental Protection Agency—Great Lakes Restoration Initiative (C.G.P., Grant #00E01934), the Michigan Botanical Foundation, and Grand Valley State University’s Center for Scholarly and Creative Excellence for financial support. Further thanks and recognition to all of the herbariums and institutes working hard to make valuable historical data accessible.
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Lamar, S.K., Partridge, C.G. Combining herbarium databases and genetic methods to evaluate the invasion of a popular horticultural species, baby’s breath (Gypsophila paniculata), in the United States. Biol Invasions 23, 37–52 (2021). https://doi.org/10.1007/s10530-020-02354-x
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DOI: https://doi.org/10.1007/s10530-020-02354-x