Evolutionary Ecology

, Volume 28, Issue 2, pp 397–411 | Cite as

Phytoplankton composition modifies predator-driven life history evolution in Daphnia

  • Matthew R. Walsh
  • Kimberly J. La Pierre
  • David M. Post
Original Paper


Organisms experience competing selective pressures, which can obscure the mechanisms driving evolution. Daphniaambigua is found in lakes where a predator, the alewife (Alosa pseudoharengus) either does (anadromous) or does not (landlocked) migrate between marine and freshwater. We previously reported an association between alewife variation and life history evolution in Daphnia. However, differences in alewife migration indirectly influence phytoplankton composition for Daphnia. In ‘anadromous lakes’, Daphnia are present in the spring and experience abundant high-quality green algae. Intense predation by young-of-the-year anadromous alewife quickly eliminates these Daphnia populations by early summer. Daphnia from ‘landlocked lakes’ and lakes without alewife (‘no alewife lakes’) are present during the spring and summer and are more likely to experience high concentrations of sub-optimal cyanobacteria during the summer. To explore links between predation, resources, and prey evolution, we reared third-generation laboratory-born Daphnia from all lake types on increasing cyanobacteria concentrations. We observed several significant ‘lake type × resource’ interactions whereby the differences among lake types depended upon cyanobacteria concentrations. Daphnia from anadromous lakes developed faster, were larger at maturation, produced more offspring, and had higher intrinsic rates of increase in the absence of cyanobacteria. Such trends disappeared or reversed as cyanobacteria concentration was increased because Daphnia from anadromous lakes were more strongly influenced by the presence of cyanobacteria. Our results argue that alewife migration and phytoplankton composition both play a role in Daphnia evolution.


Phenotypic plasticity Predator–prey Cyanobacteria Local adaptation 

Supplementary material

10682_2013_9666_MOESM1_ESM.docx (34 kb)
Supplementary material (DOCX 34 kb)


  1. Arnold DE (1971) Ingestion, assimilation, survival, and reproduction of Daphnia pulex fed seven species of blue green algae. Limnol Oceanogr 16:906–920CrossRefGoogle Scholar
  2. Barrett RDH, MacLean RC, Bell G (2005) Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am Nat 166:470–480PubMedCrossRefGoogle Scholar
  3. Bierbaum TJ, Mueller LD, Ayala FJ (1989) Density-dependent evolution of life history characteristics in Drosophila melanogaster. Evolution 43:382–392CrossRefGoogle Scholar
  4. Blom JF, Baumann HI, Codd GA, Juttner F (2006) Sensitivity and adaptation of aquatic organisms to oscillapeptin J and (D-Asp3,(E)-Dhb7) microcystin-RR. Arch Hydrobiol 167:547–559CrossRefGoogle Scholar
  5. Bochdanovits Z, de Jong G (2003) Experimental evolution in Drosophila melanogaster: interaction of temperature and food quality selection regimes. Evolution 57:1829–1837PubMedGoogle Scholar
  6. Böing W, Wagner A, Voigt H, Deppe T, Benndorf J (1998) Phytoplankton responses to grazing by Daphnia galeata in the biomanipulated Bautzen Reservoir. Hydrobiologia 389:101–114CrossRefGoogle Scholar
  7. Brett MT, Kainz M, Taipale SJ, Seshan H (2009) Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106:21197–21201PubMedCrossRefGoogle Scholar
  8. Bronikowski AM, Arnold SJ (1999) The evolutionary ecology of life history variation in the garter snake Thamnophis elegans. Ecology 80:2314–2325Google Scholar
  9. Brooks JL, Dodson SI (1965) Predation, body size, and the composition of plankton. Science 150:28–35PubMedCrossRefGoogle Scholar
  10. Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252PubMedCrossRefGoogle Scholar
  11. DeMott WR (1986) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340CrossRefGoogle Scholar
  12. DeMott WR (1989) The role of competition in zooplankton succession. In: Sommer U (ed) Plankton ecology: succession in plankton communities. Springer, Berlin, pp 195–252CrossRefGoogle Scholar
  13. DeMott WR, Zhang QX, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and 3 species of Daphnia. Limnol Oceanogr 36:1346–1357CrossRefGoogle Scholar
  14. DeMott WR, Mueller-Navarra DC (1997) The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipid emulsions. Freshw Biol 38:649–664CrossRefGoogle Scholar
  15. Desmarais KH, Tessier AJ (1999) Performance tradeoff across a natural resource gradient. Oecologia 120:137–146CrossRefGoogle Scholar
  16. Diamond SE, Kingsolver JG (2012) Host plant adaptation and the evolution of thermal reaction norms. Oecologia 169:353–360PubMedCrossRefGoogle Scholar
  17. Falconer DS, Latyszewski M (1952) The environment in relation to selection for size in mice. J Genet 51:67–80CrossRefGoogle Scholar
  18. Fox CW, Mousseau TA (1998) Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 159–177Google Scholar
  19. Ghadouani A, Pinel-Alloul B, Plath K, Codd GA, Lampert W (2004) Effects of Microcystis aeruginosa and purified microcystin-LR on the feeding behavior of Daphnia pulicaria. Limnol Oceanogr 49:666–679CrossRefGoogle Scholar
  20. Ghalambor CK, Reznick DN, Walker JA (2004) Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). Am Nat 164:38–50PubMedCrossRefGoogle Scholar
  21. Gilbert JJ (1990) Differential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications. Ecology 71:1727–1740CrossRefGoogle Scholar
  22. Gotelli NJ (1998) A primer of ecology. Sinauer Associates, MAGoogle Scholar
  23. Hairston NG Jr, Lampert W, Caceres CE, Holtmeier CL, Weider LJ, Gaedke U et al (1999) Rapid evolution revealed by dormant eggs. Nature 401:446CrossRefGoogle Scholar
  24. Hairston NG Jr, Holtmeier CL, Lampert W, Weider LJ, Post DM, Fischer JM et al (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55:2203–2214PubMedGoogle Scholar
  25. Hassall M, Helden A, Goldson A, Grant A (2005) Ecotypic differentiation and phenotypic plasticity in reproductive traits of Armadillidium vulgare (Isopoda: Oniscidea). Oecologia 143:51–60PubMedCrossRefGoogle Scholar
  26. Hillesheim E, Stearns SC (1991) The responses of Drosophila melanogaster to artificial selection on body weight and its phenotypic plasticity in two larval food environments. Evolution 45:1909–1923CrossRefGoogle Scholar
  27. Hillesheim E, Stearns SC (1992) Correlated responses in life-history traits to artificial selection for body weight in Drosophila melanogaster. Evolution 46:745–752CrossRefGoogle Scholar
  28. Hilton C, Walde SJ, Leonard ML (2002) Intense episodic predation by shorebirds may influence life history strategy of an intertidal amphipod. Oikos 99:368–376CrossRefGoogle Scholar
  29. Jennions MD, Telford SR (2002) Life history phenotypes in populations of Brachyrhaphis episcopi (Poeciliidae) with different predator communities. Oecologia 132:44–50CrossRefGoogle Scholar
  30. Johnson JB (2001) Adaptive life-history evolution in the livebearing fish Brachyrhaphis rhabdophora: genetic basis for parallel divergence in age and size at maturity and a test of predator induced plasticity. Evolution 55:1486–1491PubMedGoogle Scholar
  31. Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159CrossRefGoogle Scholar
  32. Lampert W (1987) Laboratory studies on zooplankton–cyanobacteria interactions. NZ J Mar Freshwat Res 21:483–490CrossRefGoogle Scholar
  33. Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318PubMedGoogle Scholar
  34. Lau J (2012) Evolutionary indirect effects of biological invasions. Oecologia 170:171–181PubMedCrossRefGoogle Scholar
  35. Lemaire V, Brusciotti S, van Gremberghe I, Vyverman W, Vanoverbeke J, De Meester L (2012) Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia. Evol Appl 5:168–182PubMedCentralCrossRefGoogle Scholar
  36. Lurling L (2003) Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnol Oceanogr 48:2214–2220CrossRefGoogle Scholar
  37. Lürling M, Van Donk E (1996) Zooplankton-induced unicellcolony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia 108:432–437CrossRefGoogle Scholar
  38. Lürling M, van Donk E (2000) Grazer–induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88:111–118CrossRefGoogle Scholar
  39. Lynch M (1980) The evolution of Cladoceran life histories. Q Rev Biol 55:23–42CrossRefGoogle Scholar
  40. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  41. Martin-Creuzberg D, Wacker A, Von Elert E (2005) Life history consequences of sterol availability in the aquatic keystone species Daphnia. Oecologia 144:362–372CrossRefGoogle Scholar
  42. Mayntz D, Toft S, Vollrath F (2003) Effects of prey quality and availability on the life history of a trap-building predator. Oikos 101:631–638CrossRefGoogle Scholar
  43. Mueller LD, Ayala FJ (1981) Trade-off between r-selection and K-selection in Drosophila populations. Proc Natl Acad Sci USA 78:1303–1305PubMedCrossRefGoogle Scholar
  44. Mueller LD, Guo P, Ayala FJ (1991) Density-dependent natural selection and trade-offs in life history traits. Science 253:433–435PubMedCrossRefGoogle Scholar
  45. Palkovacs EP, Post DM (2008) Eco-evolutionary interactions between predators and prey: can predator-induced changes to prey communities feedback to shape predator foraging traits? Evol Ecol Res 10:699–720Google Scholar
  46. Palkovacs EP, Dion KB, Post DM, Cacconne A (2008) Independent evolutionary origins of landlocked alewife populations and rapid parallel evolution of phenotypic traits. Mol Ecol 17:582–597PubMedCrossRefGoogle Scholar
  47. Porter KG, McDonough R (1984) The energetic cost of response to blue-green algal filaments by cladocerans. Limnol Oceanogr 29:365–369CrossRefGoogle Scholar
  48. Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032PubMedCrossRefGoogle Scholar
  49. Reznick D, Travis J (1996) The empirical study of adaptation in natural populations. In: Rose MR, Lauder GV (eds) Adaptation. Academic Press, San Diego, CA, pp 243–290Google Scholar
  50. Reznick DN, Butler MJ IV, Rodd FH (2001) Life history evolution in guppies. VII. The comparative ecology of high- and low-predation environments. Am Nat 157:126–140PubMedCrossRefGoogle Scholar
  51. Reznick DN, Bryant MJ, Roff D, Ghalambor CK, Ghalambor DE (2004) Effect of extrinsic mortality on the evolution of senescence in guppies. Nature 431:1095–1099PubMedCrossRefGoogle Scholar
  52. Rohrlack TK, Henning M, Kohl JG (1999) Mechanisms of the inhibitory effect of the cyanobacterium Microcystis aeruginosa on Daphnia galeata’s ingestion rate. J Plankton Res 21:1489–1500CrossRefGoogle Scholar
  53. Rohrlack TK, Dittmann E, Borner T, Christoffersen K (2001) Effects of cell-bound microcystins on survival and feeding of Daphnia spp. Appl Environ Microbiol 67:3523–3529PubMedCentralPubMedCrossRefGoogle Scholar
  54. Rohrlack TK, Edvardsen B, Skulberg R, Halstvedt CB, Utkilen HC, Ptacnik R et al (2003) Oligopeptide chemotypes of the toxic freshwater cyanobacterium Planktothrix can form subpopulations with dissimilar ecological traits. Limnol Oceanogr 53:1279–1293CrossRefGoogle Scholar
  55. Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570CrossRefGoogle Scholar
  56. Sarnelle O, Gustafsson S, Hansson L (2010) Effects of cyanobacteria on fitness components of the herbivore Daphnia. J Plankton Res 32:471–477CrossRefGoogle Scholar
  57. Schatz GS, McCauley E (2007) Foraging behavior by Daphnia in stoichiometric gradients of food quality. Oecologia 153:1021–1030PubMedCrossRefGoogle Scholar
  58. Schindler DW (1968) Feeding, assimilation, and respiration rates of Daphnia magna under various environmental conditions and their relation to production estimates. J Anim Ecol 37:369–385CrossRefGoogle Scholar
  59. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  60. Sparkes TCK (1996) Effects of predation risk on population variation in adult size in a stream-dwelling isopod. Oecologia 106:85–92CrossRefGoogle Scholar
  61. terHorst CP (2010) Evolution in response to direct and indirect ecological effects in pitcher plant iquiline communities. Am Nat 176:675–685PubMedCrossRefGoogle Scholar
  62. Tillmanns AR, Wilson AE, Pick FR, Sarnelle O (2008) Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundam Appl Limnol 171:285–295CrossRefGoogle Scholar
  63. Twombly S, Clancy N, Burns C (1998) Life history consequences of food quality in the freshwater copepod Boeckella triarticulata. Ecology 79:1711–1724Google Scholar
  64. Vijverberg J (1989) Culture techniques for studies on the growth, development, and reproduction of copepods and cladocerans under laboratory and in situ conditions. Freshw Biol 21:317–373CrossRefGoogle Scholar
  65. Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552–1558CrossRefGoogle Scholar
  66. Von Elert E, Martin-Creuzburg D, Le Coz JR (2002) Absence of sterols constrains carbon transfer between cyano-bacteria and a freshwater herbivore (Daphnia galeata). Proc R Soc Lond B 270:1209–1214CrossRefGoogle Scholar
  67. Walsh MR, Post DM (2011) Interpopulation variation in a fish predator drives evolutionary divergence in prey in lakes. Proc R Soc Lond B 278:2628–2637PubMedCentralPubMedCrossRefGoogle Scholar
  68. Walsh MR, Post DM (2012) The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia ambigua. J Evol Biol 25:80–89PubMedCrossRefGoogle Scholar
  69. Walsh MR, Reznick DN (2008) Interactions between the direct and indirect effects of predators determine life history evolution in a killifish. Proc Natl Acad Sci USA 105:594–599PubMedCrossRefGoogle Scholar
  70. Walsh MR, Reznick DN (2010) Influence of the indirect effects of guppies on life history evolution in Rivulus hartii. Evolution 64:1583–1593PubMedCrossRefGoogle Scholar
  71. Walsh MR, Reznick DN (2011) Experimentally induced life history evolution in a killifish in response to the introduction of guppies. Evolution 65:1021–1036PubMedCrossRefGoogle Scholar
  72. Walsh MR, DeLong JP, Hanley TC, Post DM (2012) A cascade of evolutionary change alters consumer resource dynamics and ecosystem function. Proc R Soc Lond B 279:3184–3192PubMedCentralPubMedCrossRefGoogle Scholar
  73. Wellborn GA (1994) Size-biased predation and prey life histories: a comparative study of freshwater amphipod populations. Ecology 75:2104–2117CrossRefGoogle Scholar
  74. Weider LJ, Makino W, Acharya K, Glenn KL, Kyle M, Urabe J, Elser JJ (2005) Genotype × environment interactions, stoichiometric food quality effects, and clonal existence in Daphnia pulex. Oecologia 143:537547CrossRefGoogle Scholar
  75. Wilson AE, Sarnelle O, Tillmanns AR (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol Oceanogr 51:1915–1924CrossRefGoogle Scholar
  76. Winer BJ (1971) Statistical principles in experimental design. McGraw-Hill, New York, NYGoogle Scholar
  77. Wootton JM (1994) The nature and consequences of indirect effects in ecological communities. Am Nat 25:443–466Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Matthew R. Walsh
    • 1
    • 2
  • Kimberly J. La Pierre
    • 1
  • David M. Post
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA
  2. 2.Department of BiologyUniversity of Texas ArlingtonArlingtonUSA

Personalised recommendations