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Local adaptation in adult feeding preference and juvenile performance in the generalist herbivore Idotea balthica

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Abstract

Populations can respond to environmental heterogeneity by genetic adaptation to local conditions. Evidence for local adaptation in herbivores with relatively broad host breadth is scarce, either because generalists rarely locally adapt or because fewer studies have tested for local adaptation. The marine isopod Idotea balthica, a small (<3 cm) generalist herbivore common to estuaries of the northwestern Atlantic, is found on multiple macroalgae and sea grasses north of 42°N, while more southerly populations utilize sea grass-dominated and macroalgal-poor habitats. Feeding preference assays revealed a latitudinal shift in preference hierarchy that mirrors this geographic variation in host availability. Northern populations have higher feeding preference for fresh and freeze-dried tissue of the brown macroalga Fucus vesiculosus and consumed more of its water-soluble and lipophilic extracts relative to southern populations. In contrast, southern populations have a relatively higher preference for the green macroalga Ulva linza and sea grass Zostera marina. The rank of hosts in feeding assays exhibited by northern adults (Fucus = Ulva > Zostera) and southern adults (Ulva > Fucus > Zostera) closely mirrored ranking of juvenile growth rates, suggesting that preference and performance are strongly correlated across these macrophytes. Several of our assays included isopods that had parents reared under uniform laboratory conditions, indicating that geographic differences are genetically mediated and unlikely to reflect phenotypic plasticity or maternal effects. Local adaptation in host use traits may be common in broadly distributed, generalist herbivores in marine and terrestrial systems, and will manifest itself as local shifts in the preference ranking of hosts.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Arnold TM, Targett NM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408

    Article  Google Scholar 

  • Bell TM (2009) Defining mechanisms for the maintenance of genetic diversity in the North Atlantic isopod, Idotea balthica. PhD dissertation, University of Georgia, Athens, Georgia

  • Bertness MD (2007) Atlantic shorelines: natural history and ecology. Princeton University Press, Princeton

    Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28

    Article  PubMed  Google Scholar 

  • Conover DO (1998) Local adaptation in marine fishes: evidence and implications for stock enhancement. Bull Mar Sci 62:477–493

    Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

    Google Scholar 

  • Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:1691–1699

    Article  Google Scholar 

  • Cronin G, Lindquist N, Hay M, Fenical W (1995) Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis. Mar Ecol Prog Ser 119:265–273

    Article  Google Scholar 

  • Cruz-Rivera E, Hay ME (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218:249–266

    Article  Google Scholar 

  • Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114

    Google Scholar 

  • Duffy JE (1990) Amphipods on seaweeds: partners or pests? Oecologia 83:267–276

    Article  PubMed  CAS  Google Scholar 

  • Duffy JE, Paul VJ (1992) Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339

    Article  Google Scholar 

  • Duffy JE, Macdonald KS, Rhode JM, Parker JD (2001) Grazer diversity, functional redundancy, and productivity in sea grass beds: an experimental test. Ecology 82:2417–2434

    Article  Google Scholar 

  • Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

    Google Scholar 

  • Fox LR, Morrow PA (1981) Specialization: species property or local phenomenon? Science 211:887–893

    Article  PubMed  CAS  Google Scholar 

  • Graham MH, Edwards MS (2001) Statistical significance versus fit: estimating the importance of individual effects in analysis of variance. Oikos 93:505–513

    Article  Google Scholar 

  • Grosberg RK, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD (ed) Marine community ecology. Sinauer, Sunderland, pp 61–84

    Google Scholar 

  • Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary metabolites, evolutionary and ecological processes. Academic, San Diego, pp 371–413

    Google Scholar 

  • Hay ME, Duffy JE, Pfister CA (1987) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567–1580

    Article  CAS  Google Scholar 

  • Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726

    Article  Google Scholar 

  • Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588

    Article  PubMed  Google Scholar 

  • Jaschinski S, Sommer U (2008) Functional diversity of mesograzers in an eelgrass-epiphyte system. Mar Biol 154:475–482

    Article  Google Scholar 

  • Jenkins SR, Moore P, Burrows MT, Garbary DJ, Hawkins S, Ingolfsson A, Sebens KP, Snelgrove P, Wethey DS, Woodin SJ (2008) Comparative ecology of the North Atlantic shore: do differences in players matter for process? Ecology 89:S3–S23

    Article  PubMed  Google Scholar 

  • Jones SJ, Lima FP, Wethey DS (2010) Rising environmental temperatures and biogeography: poleward range contraction of the blue mussel, Mytilus edulis L., in the western Atlantic. J Biogeogr 37:2243–2259

    Article  Google Scholar 

  • Jormalainen V, Ramsay T (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos 118:713–722

    Article  Google Scholar 

  • Jormalainen V, Honkanen T, Heikkila N (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230

    Article  Google Scholar 

  • Jormalainen V, Honkanen T, Vesakoski O (2008) Geographical divergence in host use ability of a marine herbivore in alga-grazer interaction. Evol Ecol 22:545–559

    Article  Google Scholar 

  • Kubanek J, Lester SE, Fenical W, Hay ME (2004) Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus. Mar Ecol Prog Ser 277:79–93

    Google Scholar 

  • Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

    Article  PubMed  CAS  Google Scholar 

  • Nicotri ME (1980) Factors involved in herbivore food preference. J Exp Mar Biol Ecol 42:13–26

    Article  Google Scholar 

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Env Resour 29:31–68

    Article  Google Scholar 

  • Paul VJ, Cruz-Rivera E, Thacker R (2001) Chemical mediation of macroalgal–herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, pp 227–265

    Google Scholar 

  • Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464

    Google Scholar 

  • Poore AGB, Steinberg PD (2001) Host-plant adaptation in an herbivorous marine amphipod: genetic potential not realized in field populations. Evolution 55:68–80

    PubMed  CAS  Google Scholar 

  • Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62:21–38

    PubMed  Google Scholar 

  • Rausher MD, Papaj DR (1983) Demographic consequences of discrimination among conspecific host plants by Battus philenor butterflies. Ecology 64:1402–1410

    Article  Google Scholar 

  • Salemaa H (1987) Herbivory and microhabitat preferences of Idotea spp. (Isopoda) in the Northern Baltic Sea. Ophelia 27:1–15

    Google Scholar 

  • Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Schaffelke B, Evers D, Walhorn A (1995) Selective grazing of the isopod Idotea baltica between Fucus evanescens and F. vesiculosus from Kiel Fjord (western Baltic). Mar Biol 124:215–218

    Article  Google Scholar 

  • Singer MS (2008) Evolution ecology of polyphagy. In: Tilmon KJ (ed) The evolutionary biology of herbivorous insects: specialization, speciation, and radiation. Los Angeles, Berkeley, pp 29–39

    Google Scholar 

  • Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecol Lett 8:448–459

    Article  Google Scholar 

  • Sotka EE, Giddens H (2009) Seawater temperature alters feeding discrimination by cold-temperate but not subtropical individuals of an ectothermic herbivore. Biol Bull 216:75–84

    PubMed  Google Scholar 

  • Sotka EE, Hay ME (2002) Geographic variation among herbivore populations in tolerance for a chemically-rich seaweed. Ecology 83:2721–2735

  • Sotka EE, Reynolds PL (2011) Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts. Evol Ecol 25:1335–1355

    Article  Google Scholar 

  • Sotka EE, Wares JP, Hay ME (2003) Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution 57:2262–2276

    PubMed  Google Scholar 

  • Sotka EE, Forbey J, Horn M, Poore AGB, Raubenheimer D, Whalen KE (2009) The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems. Integr Comp Biol 49:291–313

    Article  PubMed  CAS  Google Scholar 

  • Stachowicz JJ, Bruno JF, Duffy JE (2007) Understanding the effects of marine biodiversity on communities and ecosystems. Annu Rev Ecol Evol Syst 38:739–766

    Article  Google Scholar 

  • Steinberg PD, VanAltena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    Article  Google Scholar 

  • Stern JL, Hagerman AE, Steinberg PD, Mason PK (1996) Phlorotannin-protein interactions. J Chem Ecol 22:1877–1899

    Article  CAS  Google Scholar 

  • Sword GA, Dopman EB (1999) Developmental specialization and geographic structure of host plant use in a polyphagous grasshopper, Schistocerca emarginata (=lineata) (Orthoptera: Acrididae). Oecologia 120:437–445

    Article  Google Scholar 

  • Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205

    Article  CAS  Google Scholar 

  • Taylor RB, Brown PJ (2006) Herbivory in the gammarid amphipod Aora typica: relationships between consumption rates, performance and abundance across ten seaweed species. Mar Biol 149:455–463

    Article  Google Scholar 

  • Taylor R, Sotka E, Hay M (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76

    Article  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp App 47:3–14

    Article  Google Scholar 

  • Thompson JN (1993) Preference hierarchies and the origin of geographic specialization in host use in swallowtail butterflies. Evolution 47:1585–1594

    Article  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663

    Article  Google Scholar 

  • Vandendriessche S, Keersmaecker G, Vincx M, Degraer S (2006) Food and habitat choice in floating seaweed clumps: the obligate opportunistic nature of the associated macrofauna. Mar Biol 149:1499–1507

    Article  Google Scholar 

  • Vesakoski O, Bostrom C, Ramsay T, Jormalainen V (2008) Sexual and local divergence in host exploitation in the marine herbivore Idotea baltica (Pallas). J Exp Mar Biol Ecol 367:118–126

    Article  Google Scholar 

  • Vesakoski O, Rautanen J, Jormalainen V, Ramsay T (2009) Divergence in host use ability of a marine herbivore from two habitat types. J Evol Biol 22:1545–1555

    Article  PubMed  Google Scholar 

  • Wares JP (2001) Intraspecific variation and geographic isolation in Idotea balthica. J Crustacean Biol 21:1007–1013

    Article  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469

    PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank John Wares, Geoff Trussell, Northeastern University’s Marine Science Center, Meredith Doellman, Elizabeth Bryson, Timothy Dwyer, Catherine Matassa, Anna Manyak, Jeremy Long, Rachael Blake, and Nicole Rohr for logistical support. We would also like to thank Viejo Jormalainen for his constructive comments as well as the National Science Foundation (DEB-0919064) for funding. This is Grice Publication number 385.

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Correspondence to Tina M. Bell.

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Communicated by Anssi Laurila.

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Bell, T.M., Sotka, E.E. Local adaptation in adult feeding preference and juvenile performance in the generalist herbivore Idotea balthica . Oecologia 170, 383–393 (2012). https://doi.org/10.1007/s00442-012-2302-3

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