Evolutionary Ecology

, Volume 22, Issue 4, pp 545–559 | Cite as

Geographical divergence in host use ability of a marine herbivore in alga–grazer interaction

  • Veijo Jormalainen
  • Tuija Honkanen
  • Outi Vesakoski
Original Paper


When the selective environment differs geographically, local herbivore populations may diverge in their host use ability and adapt locally to exploit the sympatric host population. We tested whether populations of the marine generalist herbivore Idotea baltica have diverged in host us ability and whether they locally adapted to exploit the sympatric population of their main host species, the bladderwrack Fucus vesiculosus. We fed isopods from three local populations reciprocally with the sympatric and two allopatric populations of the host. The bladderwrack populations varied in their quality as food for isopods suggesting variation in the selective environment. The ability to exploit the main host showed considerable divergence among the isopod populations. There was no significant interaction between host and isopod origin, indicating that the patterns observed in the reciprocal feeding experiment could be explained by differences in overall suitability of the hosts and differences in overall performance of the isopod populations. Isopod population that was sympatric to a bladderwrack population with low phlorotannin content showed high performance on the algae from the sympatric but low performance on the algae from the two allopatric populations. Performance of isopods, especially in this population, decreased quickly with the increasing phlorotannin content of food algae. We therefore hypothesize that the isopods adapted to a low phlorotannin content were unable to utilize high-phlorotannin algae efficiently. Isopod populations sympatric to the high-phlorotannin bladderwrack populations may be generally better adapted to deal with phlorotannins, being thereby able to utilize a range of bladderwrack populations.


Evolutionary divergence Local adaptation Herbivory Selective mosaic Phlorotannins 



We are grateful to Janne Eränen, Meri Lindqvist and Simo Rintakoski for help in the experiment, Riitta Koivikko and Krista Tulonen for chemical analyses, Fiia Haavisto for preparing the map, and the Archipelago Research Institute (University of Turku) for facilities. This research was financed by the Academy of Finland (Project 53832, BIREME) and the Wihuri Foundation (TH).


  1. Arnold TM, Targett NM (1998) Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. J Chem Ecol 24:577CrossRefGoogle Scholar
  2. Bergelson J, Dwyer G, Emerson JJ (2001) Models and data on plant-enemy coevolution. Ann Rev Gen 35:469–499CrossRefGoogle Scholar
  3. Boecklen WJ, Mopper S (1998) Local adaptation in specialist herbivores: theory and evidence. In: Mopper S, Straus SY (eds) Genetic structure and local adaptation in natural insect populations. Chapman & Hall, New York, pp 64–88Google Scholar
  4. Borowsky B (1987) Laboratory studies of the pattern of reproduction of the Isopod Crustacean Idotea baltica. Fishery Bull 85:377–380Google Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  6. Coyer JA, Peters AF, Stam WT, Olsen JL (2003) Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe. Mol Ecol 12:1817–1829PubMedCrossRefGoogle Scholar
  7. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  8. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  9. Gomulkiewicz R, Thompson JN, Holt RD, Nuismer SL, Hochberg ME (2000) Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am Nat 156:156–174PubMedCrossRefGoogle Scholar
  10. Haahtela I (1978) Morphology as evidence of maturity in Isopod Crustacea, as exemplified by Mesidotea entomon (L.). Ann Zool Fennici 15:186–190Google Scholar
  11. Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defences against herbivores. Trends Ecol Evol 6:362–365CrossRefGoogle Scholar
  12. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal GA, Berenbaum M (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, San Diego, pp 371–413Google Scholar
  13. Hemmi A, Honkanen T, Jormalainen V (2004) Inducible resistance to herbivory in Fucus vesiculosus—duration, spreading and variation with nutrient availability. Mar Ecol Prog Ser 273:109–120CrossRefGoogle Scholar
  14. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064Google Scholar
  15. Hemmi A, Jormalainen V (2004a) Genetic and environmental variation in performance of a marine isopod: effects of eutrophication. Oecologia 140:302–311PubMedCrossRefGoogle Scholar
  16. Hemmi A, Jormalainen V (2004b) Geographic covariation of chemical quality of the host alga Fucus vesiculosus with fitness of the herbivorous isopod Idotea baltica. Mar Biol 145:759–768Google Scholar
  17. Honkanen T, Jormalainen V, Hemmi A, Mäkinen A, Heikkilä N (2002) Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 9:332–338Google Scholar
  18. Jakobsson A, Dinnetz P (2005) Local adaptation and the effects of isolation and population size—the semelparous perennial Carlina vulgaris as a study case. Evol Ecol 19:449–466CrossRefGoogle Scholar
  19. Jormalainen V, Honkanen T (2004) Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus. J Evol Biol 17:807–820PubMedCrossRefGoogle Scholar
  20. Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230CrossRefGoogle Scholar
  21. Jormalainen V, Honkanen T, Koivikko R, Eränen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650CrossRefGoogle Scholar
  22. Jormalainen V, Honkanen T, Vesakoski O, Koivikko R (2005) Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas). J Exp Mar Biol Ecol 317:143–157CrossRefGoogle Scholar
  23. Jormalainen V, Merilaita S, Tuomi J (1995) Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica (Pallas). Biol J Linn Soc 55:45–68CrossRefGoogle Scholar
  24. Kaltz O, Gandon S, Michalakis Y, Shykoff JA (1999) Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: evidence from a cross-inoculation experiment. Evolution 53:395–407CrossRefGoogle Scholar
  25. Kaltz O, Shykoff JA (1998) Local adaptation in host-parasite systems. Heredity 81:361–370CrossRefGoogle Scholar
  26. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  27. Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195–212PubMedCrossRefGoogle Scholar
  28. Lajeunesse MJ, Forbes MR (2002) Host range and local parasite adaptation. Proc R Soc Lond B 269:703–710CrossRefGoogle Scholar
  29. Merilaita S (2001) Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica. Evol Ecol 15:103–116CrossRefGoogle Scholar
  30. Morgan AD, Gandon S, Buckling A (2005) The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253–256PubMedCrossRefGoogle Scholar
  31. Nuismer SL (2006) Parasite local adaptation in a geographic mosaic. Evolution 60:24–30PubMedGoogle Scholar
  32. Nuismer SL, Thompson JN, Gomulkiewicz R (1999) Gene flow and geographically structured coevolution. Proc R Soc Lond B 266:605–609CrossRefGoogle Scholar
  33. Poore AGB, Steinberg PD (2001) Host-plant adaptation in an herbivorous marine amphipod: genetic potential not realized in field populations. Evolution 55:68–80PubMedGoogle Scholar
  34. Salemaa H (1978) Geographical variability in the colour polymorphism of Idotea baltica (Isopoda) in the northern Baltic. Hereditas 88:165–182PubMedCrossRefGoogle Scholar
  35. Salemaa H (1987) Herbivory and microhabitat preferences of Idotea spp. (Isopoda) in the northern Baltic Sea. Ophelia 27:1–15Google Scholar
  36. SAS Institute (1999) SAS/STAT User’s Guide, Version 8. SAS Institute Inc., Cary, NCGoogle Scholar
  37. Schultz JC (1988) Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69:896–897CrossRefGoogle Scholar
  38. Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecol Lett 8:448–459CrossRefGoogle Scholar
  39. Sotka EE, Hay ME (2002) Geographic variation among herbivore populations in tolerance for a chemically rich seaweed. Ecology 83:2721–2735CrossRefGoogle Scholar
  40. Sotka EE, Hay ME, Thomas JD (1999) Host-plant specialization by a non-herbivorous amphipod: advantages for the amphipod and costs for the seaweed. Oecologia 118:471–482CrossRefGoogle Scholar
  41. Sotka EE, Wares JP, Hay ME (2003) Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution 57:2262–2276PubMedGoogle Scholar
  42. Stern JL, Hagerman AE, Steinberg PD, Mason PK (1996) Phlorotannin-protein interactions. J Chem Ecol 22:1877–1899CrossRefGoogle Scholar
  43. Targett NM, Arnold TM (2001) Effects of secondary metabolites on digestion in marine herbivores. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, pp 391–412Google Scholar
  44. Tatarenkov A, Bergstrom L, Jonsson RB, Serrao EA, Kautsky L, Johannesson K (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651PubMedCrossRefGoogle Scholar
  45. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  46. Thompson JN, Cunningham BM (2002) Geographic structure and dynamics of coevolutionary selection. Nature 417:735–738PubMedCrossRefGoogle Scholar
  47. Van Zandt PA, Mopper S (1998) A meta-analysis of adaptive deme formation in phytophagous insect populations. Am Nat 152:595–604CrossRefPubMedGoogle Scholar
  48. Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: Methods for marine benthic ecology. Int Rev Hydrobiol 85:359–375CrossRefGoogle Scholar
  49. Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806–815PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Veijo Jormalainen
    • 1
  • Tuija Honkanen
    • 1
  • Outi Vesakoski
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations