Mothers forewarn offspring about predators: A transgenerational maternal effect on behavior

American Naturalist

Volumn 175, Issue 3, 2010, Pages 382-390

  Storm, Jonathan J ^a   Lima, Steven L ^a  

^a INDIANA STATE UNIVERSITY   (United States)

Author keywords

Antipredator behavior; Chemical cues; Crickets; Maternal effects; Wolf spiders

Indexed keywords

ANTIPREDATOR DEFENSE; BEHAVIORAL ECOLOGY; CHEMICAL CUE; CRICKET; MATERNAL EFFECT; POPULATION DENSITY; PREDATION RISK; SPIDER; SURVIVAL;

ANIMAL; ANIMAL BEHAVIOR; ASSOCIATION; CHEMISTRY; ECOSYSTEM; FEMALE; GRYLLIDAE; MATERNAL BEHAVIOR; PHYSIOLOGY; PREDATION; REVIEW; SPIDER; STIMULATION;

ANIMALS; BEHAVIOR, ANIMAL; CUES; ECOSYSTEM; FEMALE; GRYLLIDAE; MATERNAL BEHAVIOR; PREDATORY BEHAVIOR; SPIDERS; STIMULATION, CHEMICAL;

ARANEAE; GRYLLIDAE; GRYLLINAE; GRYLLUS PENNSYLVANICUS; HOGNA; HOGNA HELLUO; LYCOSIDAE;

EID: 77949523063     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/650443     Document Type: Review

References (41)

1. Agrawal, A. A. 2000. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493-500.
2. Agrawal, A. A., C. Laforsch, and R. Tollrian. 1999. Transgenerational induction of defences in animals and plants. Nature 401:60-63.
3. Andersen, D. H., C. Pertoldi, V. Scali, and V. Loeschcke. 2005. Heat stress and age induced maternal effects on wing size and shape in parthenogenetic Drosophila mercatorum. Journal of Evolutionary Biology 18:884-892.
4. Bailey, W. J., and S. Haythornthwaite. 1998. Risks of calling by the field cricket Teleogryllus oceanicus: potential predation by Australian long-eared bats. Journal of Zoology 244:505-513.
5. Biard, C., P. F. Surai, and A. P. Møller. 2007. An analysis of pre-and post-hatching maternal effects mediated by carotenoids in the blue tit. Journal of Evolutionary Biology 20:326-339.
6. Bossdorf, O., C. L. Richards, and M. Pigliucci. 2008. Epigenetics for ecologists. Ecology Letters 11:106-115.
7. Crews, D., A. C. Gore, T. S. Hsu, N. L. Dangleben, M. Spinetta, T. Schallert, M. D. Anway, and M. K. Skinner. 2007. Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences of the USA 104:5942-5946.
8. Curio, E., U. Ernst, and W. Vieth. 1978. Cultural transmission of enemy recognition: one function of mobbing. Science 202:899-901.
9. Fish, E. W., D. Shahrokh, R. Bagot, C. Caldji, T. Bredy, M. Szyf, and M. J. Meaney. 2004. Epigenetic programming of stress responses through variations in maternal care. Pages 167-180 in J. Devine, J. Gilligan, and Klaus A. Miczek, eds. Youth violence: scientific approaches to prevention. Annals of the New York Academy of Sciences. New York Academy of Sciences, New York.
10. Gilbert, J. J. 1966. Rotifer ecology and embryological induction. Science 151:1234-1237.
11. Griffin, A. S. 2004. Social learning about predators: a review and prospectus. Learning and Behavior 32:131-140.
12. Grindstaff, J. L., D. Hasselquist, J. A. Nilsson, M. Sandell, H. G. Smith, and M. Stjernman. 2006. Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proceedings of the Royal Society B: Biological Sciences 273:2551-2557.
13. Groothuis, T. G. G., and N. Von Engelhardt. 2005. Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Pages 168-180 in W. Goymann, S. Jenni-Eirmann, and U. Bauchinger, eds. Bird hormones and bird migrations: analyzing hormones in droppings and egg yolks and assessing adaptations in long-distance migration. Annals of the New York Academy of Sciences. New York Academy of Sciences, New Yo r k.
14. Harper, L. V. 2005. Epigenetic inheritance and the intergenerational transfer of experience. Psychological Bulletin 131:340-360.
15. Harvell, C. D., and R. Tollrian. 1999. Why inducible defenses? Pages 3-9 in R. Tollrian and C. D. Harvell, eds. The ecology and evolution of inducible defenses. Princeton University Press, Princeton, NJ.
16. Hedrick, A. V., and R. Kortet. 2006. Hiding behaviour in two cricket populations that differ in predation pressure. Animal Behaviour 72:1111-1118.
17. Hoverman, J. T., and R. A. Relyea. 2007. How flexible is phenotypic plasticity? developmental windows for trait induction and reversal. Ecology 88:693-705.
18. Kishida, O., and K. Nishimura. 2006. Flexible architecture of induc-ible morphological plasticity. Journal of Animal Ecology 75:705-712.
19. Kishida, O., Y. Mizuta, and K. Nishimura. 2006. Reciprocal phe-notypic plasticity in a predator-prey interaction between larval amphibians. Ecology 87:1599-1604.
20. Kortet, R., and A. Hedrick. 2004. Detection of the spider predator Hololena nedra by naive juvenile field crickets (Gryllus integer) using indirect cues. Behaviour 141:1189-1196.
21. Marshall, D. J., and T. Uller. 2007. When is a maternal effect adaptive? Oikos 116:1957-1963.
22. McCormick, M. I. 2006. Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87:1104-1109.
23. Meaney, M. J. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24:1161-1192.
24. Mondor, E. B., J. A. Rosenheim, and J. F. Addicott. 2005. Predator-induced transgenerational phenotypic plasticity in the cotton aphid. Oecologia (Berlin) 142:104-108.
25. Moret, Y. 2006. "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society B: Biological Sciences 273:1399-1405.
26. Podjasek, J. O, L. M. Bosnjak, D. J. Brooker, and E. B. Mondor. 2005. Alarm pheromone induces a transgenerational wing poly-phenism in the pea aphid, Acyrthosiphon pisum. Canadian Journal of Zoology 83:1138-1141.
27. Rakshpal, R. 1962. Diapause in eggs of Gryllus pennsylvanicus Bur-meister (Orthoptera-Gryllidae). Canadian Journal of Zoology 40: 179-194.
28. Rasanen, K., and L. E. B. Kruuk. 2007. Maternal effects and evolution at ecological time-scales. Functional Ecology 21:408-421.
29. Reinhold, K. 2002. Maternal effects and the evolution of behavioral and morphological characters: a literature review indicates the importance of extended maternal care. Journal of Heredity 93: 400-405.
30. Relyea, R. A. 2003. Predators come and predators go: the reversibility of predator-induced traits. Ecology 84:1840-1848.
31. Roeder, T. 1999. Octopamine in invertebrates. Progress in Neuro-biology 59:533-561.
32. Schmitz, O. J., A. P. Beckerman, and K. M. Obrien. 1997. Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388-1399.
33. Shine, R., and S. J. Downes. 1999. Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia (Berlin) 119:1-8.
34. Stevenson, P. A., V. Dyakonova, J. Rillich, and K. Schildberger. 2005. Octopamine and experience-dependent modulation of aggression in crickets. Journal of Neuroscience 25:1431-1441.
35. Storm, J. J., and S. L. Lima. 2008. Predator-nä?ve fall field crickets respond to the chemical cues of wolf spiders. Canadian Journal of Zoology 86:1259-1263.
36. Szyf, M., I. Weaver, and M. Meaney. 2007. Maternal care, the epi-genome and phenotypic differences in behavior. Reproductive Toxicology 24:9-19.
37. Tschirren, B., P. S. Fitze, and H. Richner. 2007. Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? American Naturalist 169:87-93.
38. Uller, T., and M. Olsson. 2006. Direct exposure to corticosterone during embryonic development influences behaviour in an ovo-viviparous lizard. Ethology 112:390-397.
39. Weisser, W. W., C. Braendle, and N. Minoretti. 1999. Predator-induced morphological shift in the pea aphid. Proceedings of the Royal Society B: Biological Sciences 266:1175-1181.
40. Wolf, J. B., and M. J. Wade. 2009. What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B: Biological Sciences 364:1107-1115.
41. Zhang, T. Y., C. Parent, I. Weaver, and M. J. Meaney. 2004. Maternal programming of individual differences in defensive responses in the rat. Pages 85-103 in R. Yehuda and B. S. McEwen, eds. Bio-behavioral stress response: protective and damaging effects. Annals of the New York Academy of Sciences. New York Academy of Sciences, New York.