Biological Invasions

, Volume 20, Issue 1, pp 235–250 | Cite as

Local differentiation in the defensive morphology of an invasive zooplankton species is not genetically based

  • Giuseppe E. FiorinoEmail author
  • Andrew G. McAdam
Original Paper


Evolutionary changes in functional traits represent one possible reason why exotic species spread to become invasive, but empirical studies of the mechanisms driving phenotypic differentiation between populations of invasive species are rare. This study tested whether differences in distal spine length among populations of the invasive cladoceran, Bythotrephes longimanus, could be explained by local adaptation or phenotypic plasticity. We collected Bythotrephes from six lakes and found that distal spine lengths and natural selection on distal spine length differed among populations, but were unrelated to the gape-limitation of the dominant fish predator in the lake from which they were collected. A common garden experiment revealed significant genetic and maternal variation for distal spine length, but phenotypic differences among populations were not genetically based. Phenotypic differences among lakes in this ecologically important trait are, therefore, the result of plasticity and not local adaptation, despite spatially variable selection on this heritable trait. The ability of Bythotrephes to plastically adjust distal spine length may explain the success of this species at invading lake ecosystems with diverse biotic environments.


Bythotrephes longimanus Cladoceran Common garden experiment Invasive species Local adaptation Phenotypic plasticity 



We thank Teresa Crease and Beren Robinson for insightful comments, and for providing field and lab equipment. The Dorset Environmental Science Centre (DESC) provided a climate controlled facility. James Rusak (DESC) and Matt Cornish (Hagen Aqualab) assisted with lab set-up. Andrea Miehls helped with Bythotrephes collection and culturing protocols. Guang Zhang assisted with field work. Emily De Freitas, Evan McKenzie, Kaileigh Watson, Katelyn Cross, Kirsten Bradford, Marissa Skinner, Mary Paquet, Meera Navaratnam, Ronena Wolach, and Yu Jin Song assisted with data collection.


This study was funded by an Ontario Ministry of Research and Innovation Early Researcher Award to Andrew McAdam (ER08-05-119), a Natural Sciences and Engineering Research Council Discovery Grant to Andrew McAdam (RGPIN371579-2009), and an Ontario Graduate Scholarship to Giuseppe Fiorino.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2017_1530_MOESM1_ESM.docx (787 kb)
Supplementary material 1 (DOCX 787 kb)


  1. Abdi H, Williams LJ (2010) Tukey’s honestly significant difference (HSD) test. In: Salkind NJ (ed) Encyclopedia of research methods. Sage, Thousand OaksGoogle Scholar
  2. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42Google Scholar
  3. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  4. Barnhisel DR (1991a) The caudal appendage of the cladoceran Bythotrephes cederstroemi as defense against young fish. J Plankton Res 13:529–537CrossRefGoogle Scholar
  5. Barnhisel DR (1991b) Zooplankton spine induces aversion in small fish predators. Oecologia 88:444–450CrossRefPubMedGoogle Scholar
  6. Barnhisel DR, Harvey HA (1995) Size-specific fish avoidance of the spined crustacean Bythotrephes: field support for laboratory predictions. Can J Fish Aquat Sci 52:768–775CrossRefGoogle Scholar
  7. Bell G (2010) Fluctuating selection: the perpetual renewal of adaptation in variable environments. Philos Trans R Soc Lond B Biol Sci 365:87–97CrossRefPubMedPubMedCentralGoogle Scholar
  8. Branstrator DK (2005) Contrasting life histories of the predatory cladocerans Leptodora kindtii and Bythotrephes longimanus. J Plankton Res 27:569–585CrossRefGoogle Scholar
  9. Bunnell DB, Davis BM, Warner DM, Chriscinske MA, Roseman EF (2011) Planktivory in the changing Lake Huron zooplankton community: Bythotrephes consumption exceeds that of Mysis and fish. Freshw Biol 56:1281–1296CrossRefGoogle Scholar
  10. Burkhardt S (1994) Seasonal size variation in the predatory cladoceran Bythotrephes cederstroemii in Lake Michigan. Freshw Biol 31:97–108CrossRefGoogle Scholar
  11. Colautti RI, Manca M, Viljanen M, Ketelaars HAM, Bürgi H, Macisaac HJ, Heath DD (2005) Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Mol Ecol 14:1869–1879CrossRefPubMedGoogle Scholar
  12. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  13. Day T, Abrams PA, Chase JM (2002) The role of size-specific predation in the evolution and diversification of prey life histories. Evolution 56:877–887CrossRefPubMedGoogle Scholar
  14. Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (1989) Biological Invasions: a global perspective. Wiley, New YorkGoogle Scholar
  15. Dybdahl MF, Kane SL (2005) Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 86:1592–1601CrossRefGoogle Scholar
  16. Dzialowski AR, Lennon JT, O’Brien WJ, Smith VH (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshw Biol 48:1593–1602CrossRefGoogle Scholar
  17. Evans DO, Loftus DH (1987) Colonization of inland lakes in the Great Lakes region by rainbow smelt, Osmerus mordax: their freshwater niche and effects on indigenous fishes. Can J Fish Aquat Sci 44:249–266CrossRefGoogle Scholar
  18. Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135CrossRefPubMedGoogle Scholar
  19. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, HarlowGoogle Scholar
  20. Godoy O, Saldana A, Fuentes N, Valladares F, Gianoli E (2011) Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biol Invasions 13:1615–1625CrossRefGoogle Scholar
  21. Grigorovich IA, Pashkova OV, Gromova YF, van Overdijk CDA (1998) Bythotrephes longimanus in the commonwealth of independent states: variability, distribution and ecology. Hydrobiologia 379:183–198CrossRefGoogle Scholar
  22. Hovius JT, Beisner BE, McCann KS (2006) Epilimnetic rotifer community responses to Bythotrephes longimanus invasion in Canadian shield lakes. Limnol Oceanogr 51:1004–1012CrossRefGoogle Scholar
  23. Johannsson OE, Mills EL, O’Gorman R (1991) Changes in the nearshore and offshore zooplankton communities in Lake Ontario: 1981–1988. Can J Fish Aquat Sci 48:1546–1557CrossRefGoogle Scholar
  24. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  25. Kelly NE, Yan ND, Walseng B, Hessen DO (2013) Differential short- and long-term effects of an invertebrate predator on zooplankton communities in invaded and native lakes. Divers Distrib 19:396–410CrossRefGoogle Scholar
  26. Kim N, Yan ND (2010) Methods for rearing the invasive zooplankter Bythotrephes in the laboratory. Limnol Oceanogr Methods 8:552–561CrossRefGoogle Scholar
  27. Kim N, Yan ND (2013) Food limitation impacts life history of the predatory cladoceran Bythotrephes longimanus, an invader to North America. Hydrobiologia 715:213–224CrossRefGoogle Scholar
  28. Kingsolver JG, Diamond SE (2011) Phenotypic selection in natural populations: what limits directional selection? Am Nat 177:346–357CrossRefPubMedGoogle Scholar
  29. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gilbert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261CrossRefPubMedGoogle Scholar
  30. Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070CrossRefGoogle Scholar
  31. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  32. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefPubMedGoogle Scholar
  33. Lüning J (1992) Phenotypic plasticity of Daphnia pulex in the presence of invertebrate predators: morphological and life history responses. Oecologia 92:383–390CrossRefPubMedGoogle Scholar
  34. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  35. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  36. Merilä J, Sheldon BC, Kruuk LEB (2001) Explaining stasis: microevolutionary studies in natural populations. Genetica 112–113:199–222CrossRefPubMedGoogle Scholar
  37. Miehls ALJ, Peacor SD, McAdam AG (2012) Genetic and maternal effects on tail spine and body length in the invasive spiny water flea (Bythotrephes longimanus). Evol Appl 5:306–316CrossRefPubMedGoogle Scholar
  38. Miehls ALJ, McAdam AG, Bourdeau PE, Peacor SD (2013) Plastic response to a proxy cue of predation risk when direct cues are unreliable. Ecology 94:2237–2248CrossRefPubMedGoogle Scholar
  39. Miehls ALJ, Peacor SD, McAdam AG (2014) Gape-limited predators as agents of selection on the defensive morphology of an invasive invertebrate. Evolution 68:2633–2643CrossRefPubMedGoogle Scholar
  40. Miehls ALJ, Peacor SD, Valliant L, McAdam AG (2015) Evolutionary stasis despite selection on a heritable trait in an invasive zooplankton. J Evol Biol 28:1091–1102CrossRefPubMedGoogle Scholar
  41. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407CrossRefPubMedGoogle Scholar
  43. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197CrossRefPubMedGoogle Scholar
  44. Novak SJ (2007) The role of evolution in the invasion process. Proc Natl Acad Sci USA 104:3671–3672CrossRefPubMedPubMedCentralGoogle Scholar
  45. Parker IM, Rodriguez J, Loik ME (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conserv Biol 17:59–72CrossRefGoogle Scholar
  46. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467CrossRefPubMedGoogle Scholar
  47. Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486CrossRefPubMedGoogle Scholar
  48. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New YorkCrossRefGoogle Scholar
  49. Pinheiro JC, Bates DM, DebRoy S, Sarkar D, Core Team R (2015) nlme: Linear and nonlinear mixed effects models. R Package Version 3:1–121Google Scholar
  50. Pothoven SA, Fahnenstiel GL, Vanderploeg HA (2003) Population characteristics of Bythotrephes in Lake Michigan. J Great Lakes Res 29:145–156CrossRefGoogle Scholar
  51. Pothoven SA, Vanderploeg HA, Cavaletto JF, Krueger DM, Mason DM, Brandt SB (2007) Alewife planktivory controls the abundance of two invasive predatory cladocerans in Lake Michigan. Freshw Biol 52:561–573CrossRefGoogle Scholar
  52. Pothoven SA, Vanderploeg HA, Warner DM, Schaeffer JS, Ludsin SA, Claramunt RM, Nalepa TF (2012) Influences on Bythotrephes longimanus life-history characteristics in the Great Lakes. J Great Lakes Res 38:134–141CrossRefGoogle Scholar
  53. Roff D (2002) Life history evolution. Sinauer Associates, SunderlandGoogle Scholar
  54. Schluter D, Price TD, Rowe L (1991) Conflicting selection pressures and life history trade-offs. Proc R Soc Lond Ser B Bio 246:11–17CrossRefGoogle Scholar
  55. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  56. Si C-C, Dai Z-C, Lin Y, Qi S-S, Huang P, Miao S-L, Du D-L (2014) Local adaptation and phenotypic plasticity both occurred in Wedelia trilobata invasion across a tropical island. Biol Invasions 16:2323–2337CrossRefGoogle Scholar
  57. Siepielski AM, DiBattista JD, Carlson SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276CrossRefPubMedGoogle Scholar
  58. Straile D, Halbich A (2000) Life history and multiple antipredator defenses of an invertebrate pelagic predator, Bythotrephes longimanus. Ecology 81:150–163CrossRefGoogle Scholar
  59. Strecker AL, Arnott SE, Yan ND, Girard R (2006) Variation in the response of crustacean zooplankton species richness and composition to the invasive predator Bythotrephes longimanus. Can J Fish Aquat Sci 63:2126–2136CrossRefGoogle Scholar
  60. Therriault TW, Grigorovich IA, Cristescu ME, Ketelaars HAM, Viljanen M, Heath DD, Macisaac HJ (2002) Taxonomic resolution of the genus Bythotrephes Leydig using molecular markers and re-evaluation of its global distribution. Divers Distrib 8:67–84CrossRefGoogle Scholar
  61. Urban MC (2007) Predator size and phenology shape prey survival in temporary ponds. Oecologia 154:571–580CrossRefPubMedGoogle Scholar
  62. Urban MC (2008) Salamander evolution across a latitudinal cline in gape limited predation risk. Oikos 117:1037–1049CrossRefGoogle Scholar
  63. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  64. Wallace B (1975) Hard and soft selection revisited. Evolution 29:465–473CrossRefPubMedGoogle Scholar
  65. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  66. Young JD, Yan ND (2008) Modification of the diel vertical migration of Bythotrephes longimanus by the cold-water planktivore, Coregonus artedi. Freshw Biol 53:981–995CrossRefGoogle Scholar
  67. Yurista PM (1992) Embryonic and postembryonic development in Bythotrephes cederstoemii. Can J Fish Aquat Sci 49:1118–1125CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada

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