Abstract
Inducible defenses of prey and inducible offenses of predators are examples of adaptive phenotypic plasticity. Although evolutionary ecologists have paid considerable attention to the adaptive significances of these strategies, they have rarely focused on their evolutionary impacts on the interacting species. Because the functional phenotypes of predator and prey determine strength of interactions between the species, the inducible plasticity can modify selective pressure on trait distribution and, ultimately, trait evolution in the interacting species. We experimentally tested this hypothesis in a predator–prey system composed of salamander larvae (Hynobius retardatus) and frog tadpoles (Rana pirica) capable of expressing antagonistic inducible offensive or defensive traits, an enlarged gape in the salamander larvae and a bulgy body in the tadpoles, when predator–prey interactions are strong. We examined selection strength on the tadpole’s defensive trait by comparing survival rates of tadpoles with different defensive levels under predation pressure from offensive or non-offensive salamander larvae. Survival rates of more-defensive tadpoles were greater than those of less-defensive tadpoles only when the tadpoles were exposed to offensive salamander larvae; thus, the predator’s offensive phenotype could select for an amplified defensive phenotype in their prey. As the expression of inducible offenses by H. retardatus larvae depends greatly on the composition of its ecological community, the inducible defensive bulgy morph of R. pirica tadpoles might have evolved in response to the variable expression of the H. retardatus offensive larval phenotype.
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References
Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326
Agrawal AA, Ackerly DD, Adler F, Arnold AE, Caceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA, Power M, Schemske D, Stachowicz J, Strauss S, Turner MG, Werner E (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152
DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York
Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton
Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol 209:2377–2383
Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci USA 107:15503–15507
Hawlena D, Hughes KM, Schmitz OJ (2011) Trophic trait plasticity in response to changes in resource availability and predation risk. Funct Ecol 25:1223–1231
Iwami T, Kishida O, Nishimura K (2007) Direct and indirect induction of a compensatory phenotype that alleviates the costs of an inducible defense. PLoS One 2(10):e1084
Kerfoot WC, Sih A (1987) Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover
Kishida O, Nishimura K (2004) Bulgy tadpoles: inducible defense morph. Oecologia 140:414–421
Kishida O, Nishimura K (2005) Multiple inducible defences against multiple predators in the anuran tadpole, Rana pirica. Evol Ecol Res 7:619–631
Kishida O, Nishimura K (2006) Flexible architecture of inducible morphological plasticity. J Anim Ecol 75:705–712
Kishida O, Mizuta Y, Nishimura K (2006) Reciprocal phenotypic plasticity in a predator–prey interaction between larval amphibians. Ecology 87:1599–1604
Kishida O, Trussell GC, Nishimura K (2007) Geographic variation in a predator-induced defense and its genetic basis. Ecology 88:1948–1954
Kishida O, Trussell GC, Nishimura K (2009a) Top-down effects on antagonistic inducible defense and offense. Ecology 90:1217–1226
Kishida O, Trussell GC, Nishimura K, Ohgushi T (2009b) Inducible defenses in prey intensify predator cannibalism. Ecology 90:3150–3158
Kishida O, Trussell GC, Mougi A, Nishimura K (2010) Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology. Popul Ecol 52:37–46
Kishida O, Trussell GC, Ohno A, Kuwano S, Ikawa T, Nishimura K (2011) Predation risk suppresses the positive feedback between size structure and cannibalism. J Anim Ecol 80:1278–1287
Kondoh M (2003) Foraging adaptation and the relationship between food-web complexity and stability. Science 299:1388–1391
Kondoh M (2007) Anti-predator defence and the complexity–stability relationship of food webs. Proc R Soc B 274:1617–1624
Kopp M, Tollrian R (2003a) Trophic size polyphenism in Lembadion bullinum: costs and benefits of an inducible offense. Ecology 84:641–651
Kopp M, Tollrian R (2003b) Reciprocal phenotypic plasticity in a predator–prey system: inducible offences against inducible defences? Ecol Lett 6:742–748
Lima SL (2002) Putting predators back into behavioral predator–prey interactions. Trends Ecol Evol 17:70–75
Lively CM (1986a) Predator-induced shell dimorphism in the acorn barnacles Chtamalus anisopoma. Evolution 40:232–242
Lively CM (1986b) Competition, comparative life histories, and maintenance of shell dimorphism in a barnacle. Ecology 67:858–864
Michimae H (2006) Differentiated phenotypic plasticity in larvae of the cannibalistic salamander Hynobius retardatus. Behav Ecol Sociobiol 60:205–211
Michimae H, Wakahara M (2002) A tadpole-induced polyphenism in the salamander Hynobius retardatus. Evolution 56:2029–2038
Michimae H, Nishimura K, Tamori Y, Wakahara M (2009) Maternal effects on phenotypic plasticity in larvae of the salamander Hynobius retardatus. Oecologia 160:601–608
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692
Mori T, Kawachi H, Imai C, Sugiyama M, Kurata Y, Kishida O, Nishimura K (2009) Identification of a novel uromodulin-like gene related to predator-induced bulgy morph in anuran tadpoles by functional microarray analysis. PLoS One 4:e5936
Mougi A, Kishida O, Iwasa Y (2011) Coevolution of phenotypic plasticity in predator and prey: why are inducible offenses rarer than inducible defenses? Evolution 65:1079–1087
Ohdachi S (1994) Growth, metamorphosis, and gape-limited cannibalism and predation on tadpoles in larvae of salamanders Hynobius retardatus. Zool Sci 11:127–131
Padilla DK (2001) Food and environmental cues trigger an inducible offence. Evol Ecol Res 3:15–25
Pettersson LB, Brönmark C (1997) Density dependent costs of an inducible morphological defense in crucian carp. Ecology 78:1805–1815
Pfennig D (1990) The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia 85:101–107
Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore
Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Evol Syst 24:35–68
Smith LD, Palmer AR (1994) Effects of manipulated diet on size and performance of brachyuran crab claws. Science 264:710–712
Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago
Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton
Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454
Trussell GC, Ewanchuk PJ, Bertness MD (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245
Utsumi S (2011) Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Popul Ecol 53:23–34
Utsumi S, Ando Y, Ohgushi T (2009) Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant. Ecol Lett 12:920–929
Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102
Via S, Gomulkiewicz R, de Jong G, Scheiner SM, Schlichting CD, van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217
Vonesh JR, Osenberg CW (2003) Multi-predator effects across life-history stages: non-additivity of egg-and larval-stage predation in an African treefrog. Ecol Lett 6:503–508
Vos M, Flik BJG, Vijverberg J, Ringelberg J, Mooij WM (2002) From inducible defences to population dynamics: modelling refuge use and life history changes in Daphnia. Oikos 99:386–396
Vos M, Kooi BW, DeAngelis DL, Mooij WM (2004a) Inducible defences and the paradox of enrichment. Oikos 105:471–480
Vos M, Verschoor AM, Kooi BW, Wäckers FL, DeAngelis DL, Mooij WM (2004b) Inducible defenses and trophic structure. Ecology 85:2783–2794
Warkentin KM (1995) Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc Natl Acad Sci USA 92:3507–3510
Acknowledgments
We are very grateful to staff members of Teshio Experimental Forest of Hokkaido University for their considerable support in setting up the experiments and rearing animals. We thank Mrs. Maricar Aguilos and three anonymous reviewers for their constructive comments on our previous version of manuscript. This study was supported by a Grant-in-Aid for a Research Fellow of the Japan Society for the Promotion of Science Research Fellowship for Young Scientists (no. 2277001101) to Osamu Kishida.
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Takatsu, K., Kishida, O. An offensive predator phenotype selects for an amplified defensive phenotype in its prey. Evol Ecol 27, 1–11 (2013). https://doi.org/10.1007/s10682-012-9572-4
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DOI: https://doi.org/10.1007/s10682-012-9572-4