The invasion history of the exotic freshwater zooplankter Daphnia lumholtzi (Cladocera, Crustacea) in North America: a genetic analysis

Abstract

Daphnia lumholtzi is a planktonic crustacean native to subtropical regions in Africa, Asia and Australia. Since its invasion to the southern USA in ~1990 it has spread across North America as far north as the Laurentian Great Lakes. We assessed invasion history using microsatellite makers and to explore the influence of mean annual temperature on the genetic structure along a latitudinal gradient in North America. Genotypic data were obtained from 9 microsatellite markers for 178 individuals from 13 populations (eight populations introduced to North America and five populations in the native range). Pairwise Fst values as well as Bayesian clustering showed a strong subdivision between native and introduced populations. Bayesian clustering identified multiple genetic clusters in recently invaded locations, suggestive of multiple invasions from various sources, including Asia and Africa. Using variation partitioning, we determined the amount of variation for genetic clusters of populations in the invaded range due to mean annual air temperature and the year of first detection. The results point to a primary introduction into the southern range of North America, with a subsequent northward expansion, and multiple introductions possibly from both the native range and by secondary spread from previously-invaded locations. Separate analysis of genetic clusters within the invaded range suggests additional effects of temperature conditions on geographic genetic structure, possibly as a consequence of D. lumholtzi’s tropical origin.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Ascunce MS, Yang C-C, Oakey J, Calcaterra L, Wu W-J, Shih C-J, Goudet J, Ross KG, Shoemaker D (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068

    PubMed  CAS  Article  Google Scholar 

  2. Benzie JAH (2005) Cladocera: the genus Daphnia (including Daphniopsis). Guides to the identification of the microinvertebrates of the continental waters of the world. Backhuys, Leiden, pp 368

  3. Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616–623

    PubMed  CAS  Article  Google Scholar 

  4. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    PubMed  CAS  Article  Google Scholar 

  5. Cristescu MEA, Hebert PDN, Witt JDS, MacIsaac HJ, Grigorovich IA (2001) An invasion history for Cercopagis pengoi based on mitochondrial gene sequences. Limnol Oceanogr 46:224–229

    Article  Google Scholar 

  6. 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

    Google Scholar 

  7. Earl DA (2011) Structure harvester v0.6.1. http://taylor0.biology.ucla.edu/structureHarvester/

  8. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 19:4113–4130

    Article  Google Scholar 

  9. 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

    PubMed  CAS  Article  Google Scholar 

  10. Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253

    Article  Google Scholar 

  11. Frisch D, Weider LJ (2010) Seasonal shifts in genotype frequencies in the invasive cladoceran Daphnia lumholtzi in Lake Texoma, USA. Freshw Biol 55:1327–1336

    Article  Google Scholar 

  12. Green J (1971) Associations of Cladocera in the zooplankton of the lake sources of the White Nile. J Zool Lond 165:373–414

    Article  Google Scholar 

  13. Green J (1995) Altitudinal distribution of tropical planktonic Cladocera. Hydrobiologia 307:75–84

    Article  Google Scholar 

  14. Havel JE, Hebert PDN (1993) Daphnia lumholtzi in North America—another exotic zooplankter. Limnol Oceanogr 38:1823–1827

    Article  Google Scholar 

  15. Havel JE, Medley KA (2006) Biological invasions across spatial scales: intercontinental, regional, and local dispersal of cladoceran zooplankton. Biol Invasions 8:459–473

    Article  Google Scholar 

  16. Havel JE, Shurin JB (2004) Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnol Oceanogr 49:1229–1238

    Article  Google Scholar 

  17. Havel JE, Stelzleni-Schwent J (2000) Zooplankton community structure: the role of dispersal. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 27:3264–3268

    Google Scholar 

  18. Havel JE, Colbourne JK, Hebert PDN (2000) Reconstructing the history of intercontinental dispersal in Daphnia lumholtzi by use of genetic markers. Limnol Oceanogr 45:1414–1419

    Article  Google Scholar 

  19. Havel JE, Shurin JB, Jones JR (2002) Estimating dispersal from patterns of spread: spatial and local control of lake invasions. Ecology 83:3306–3318

    Article  Google Scholar 

  20. Hillis DM, Moritz C, Mable BK (1990) Molecular systematics. Sinauer & Associates, Sunderland, USA

  21. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    PubMed  Article  Google Scholar 

  22. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    PubMed  CAS  Article  Google Scholar 

  23. Jansen B, Geldof S, De Meester L, Orsini L (2011) Isolation and characterization of microsatellite markers in the waterflea Daphnia magna. Mol Ecol Resour 11:418–421

    PubMed  Article  Google Scholar 

  24. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. v.3.21. http://ibdws.sdsu.edu/

  25. Kelly DW, Muirhead JR, Heath DD, MacIsaac HJ (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol Ecol 15:3641–3653

    PubMed  CAS  Article  Google Scholar 

  26. Kolbe JJ, Glor RE, Schettino LRG, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    PubMed  CAS  Article  Google Scholar 

  27. Lachmuth S, Durka W, Schurr FM (2010) The making of a rapid plant invader: genetic diversity and differentiation in the native and invaded range of Senecio inaequidens. Mol Ecol 19:3952–3967

    PubMed  Article  Google Scholar 

  28. MacIsaac HJ, Grigorovich IA, Hoyle JA, Yan ND, Panov VE (1999) Invasion of Lake Ontario by the Ponto-Caspian predatory cladoceran Cercopagis pengoi. Can J Fish Aquat Sci 56:1–5

    Google Scholar 

  29. Montero-Pau J, Gomez A, Muñoz J (2008) Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnol Oceanogr Methods 6:218–222

    CAS  Article  Google Scholar 

  30. Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic-variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  31. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  32. Reusch TBH, Bolte S, Sparwel M, Moss AG, Javidpour J (2010) Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world’s most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Mol Ecol 19:2690–2699

    PubMed  CAS  Article  Google Scholar 

  33. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    PubMed  Article  Google Scholar 

  34. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  35. Routtu J, Jansen B, Colson I, De Meester L, Ebert D (2010) The first-generation Daphnia magna linkage map. BMC Genomics 11:508

    PubMed  Article  Google Scholar 

  36. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    CAS  Article  Google Scholar 

  37. Simoes NR, Robertson BA, Lansac-Toha FA, Takahashi EM, Bonecker CC, Velho LFM, Joko CY (2009) Exotic species of zooplankton in the Upper Parana River floodplain, Daphnia lumholtzi Sars, 1885 (Crustacea: Branchiopoda). Braz J Biol 69:551–558

    PubMed  CAS  Article  Google Scholar 

  38. Sorensen KH, Sterner RW (1992) Extreme cyclomorphosis in Daphnia lumholtzi. Freshw Biol 28:257–262

    Article  Google Scholar 

  39. Swar D, Fernando C (1979) Cladocera from Pokhara Valley, Nepal with notes on distribution. Hydrobiologia 66:113–128

    Article  Google Scholar 

  40. Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    PubMed  CAS  Article  Google Scholar 

  41. ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, New York

    Google Scholar 

  42. Timms BV (1973) A limnological survey of the freshwater coastal lakes of East Gippsland, Victoria. Aust J Mar Freshw Resour 24:1–20

    CAS  Article  Google Scholar 

  43. Yan ND, Leung B, Lewis MA, Peacor SD (2011) The spread, establishment and impacts of the spiny water flea, Bythotrephes longimanus, in temperate North America: a synopsis of the special issue. Biol Invasions 13:2423–2432

    Article  Google Scholar 

  44. Zanata LH, Espindola ELG, Rocha O, Pereira RHG (2003) First record of Daphnia lumholtzi (Sars, 1885), exotic Cladoceran, in Sao Paulo State (Brazil). Braz J Biol 63:717–720

    PubMed  CAS  Article  Google Scholar 

Download references

Acknowledgments

We are grateful to John Colbourne, Joachim Mergeay and Luc De Meester for sharing microsatellite primer sequences, to Robert Burdis, John Colbourne, Norman Davidson, Meghan Duffy, Wyatt Hoback, Ram Kumar, Chris Luecke, Anke Mueller-Solger, Brian Peterson, La-orsri Sanoamuang, Ron Semyalo, Jim Stoeckel and Colin van Overdijk for providing samples used in this study, and to Amy Benson, United States Geological Survey for providing us with a map of the temporal D. lumholtzi distribution in North America. DF was supported by a European Commision Outgoing International Marie Curie postdoctoral fellowship (MOIF-CT-EVOLEXOTIC 40285). We thank two anonymous reviewers for constructive comments on an earlier version of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Dagmar Frisch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 122 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Frisch, D., Havel, J.E. & Weider, L.J. The invasion history of the exotic freshwater zooplankter Daphnia lumholtzi (Cladocera, Crustacea) in North America: a genetic analysis. Biol Invasions 15, 817–828 (2013). https://doi.org/10.1007/s10530-012-0329-3

Download citation

Keywords

  • Biological invasion
  • Macrogeographic genetic structure
  • Range expansion
  • Zooplankton
  • Population genetics
  • Microsatellites