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Induced defenses and phenotypic plasticity
CORRESPONDENCE the limit of plausibility. They stress that the theones they discuss ‘are often testable by looking at existing organisms’. This explains why the presumed driving forces that may have resulted in the major transitions are not discussed in the book. Although JMSES do not declare it explicitly, the reader must conclude that the transitions were most likely the results of chance events analogous to Crick’s2 ‘frozen accident’ of codon assignments. In a recent TREEarticle, Wieser3 tried to fill the seeming lacuna of JMSES’s theory by suggesting that ‘the driving force . can only be ecological diversification. This is the quality that increases with each transition: specialization and differentiation allowing exploitation of new resources of energy and materials; ‘. It is, however, hard to imagine by what mechanism an unused or a new resource has drrven, e.g. unicellular algae to form V&ox, or prokaryotes to become eukaryotes. Clearly, exploitation of a new resource is the result rather than the cause of an evolutionary change. Following JMSES’s reasoning, Wieser’s assumption can be tested by looking at existing cases of ecological relationships between organisms. For example, it has been proved unequivocally that host-plant switching in herbivorous insects can be traced back to heritable changes in the insects’ chemoreceptors that govern host-selection behaviour4,5. However, at the present state of biological sciences one cannot imagine how the presence of a plant specres, as a possible new resource, could cause heritable changes in the insect’s chemoreceptors so that hereafter it would recognize that plant as a host! Thus, the use of a new plant species is the result of heritable changes in the insects’ plant recognrtion process. Since basic biological principles are largely independent of time and scale, It can be concluded that, although transrtions often resulted in ecological diversification, the latter per se could not have been the driving force of major transitions in evolution. Supposing the opposite would verge on Lamarckism. Looking for forces of selection that might have driven major transitions in evolution means forgetting Jacob’s6 generally accepted view that selection is not an engineer who is able to create anything, but rather a tinker who can assemble new things using only available junk. I am grateful to Prof. Ears Szathmary for a fruitful discussion on these questions,
Tibor
Jermy
Plant Protection Institute, Hungarian Academy of Sciences, PO Box 102, H-1525 Budapest, Hungary References 1 Maynard Smith, J. and Szathmaty, The Major
Transitions
E. (1995)
in Evolution,
W.H. Freeman 2 Crick. F.H.C. (1968) J. MO/ Viol. 38, 367-379 3 Wieser. W. (1997) Trends Ecol. Evol.12, 367-370 4 Jermy,T. (1993) Entomol. Exp.Appl.66, 3-12 5 Menken, S.B.J. (1996) Entomol. Exp. Appl. 80, 297-305
6 Jacob, F. (1981)
200
Copyright
Le Jeu des Possibles, 0 1998,
Elsevier
Fayard Science
Reply from W. Wieser Tibor Jermy takes me to task for calling ecological diversification a ‘driving force’ behind the ‘major transitions in evolution’. He is right. I shouldn’t have put it this way. Ecological diversification cannot be a ‘force’ for the same reason that selection cannot exert ‘pressure’. What was implied is that each transition opened up new ecological potentials that were exploited, sometimes with extraordinary rapidity, by a new class of biological systems the members of which had become units of selection. Consider my example of large metazoans, derived from unicellular organisms, colonizing the up-to-then pristine oceanic niche in which locomotion is not seriously impeded by the viscosity of water. Once organisms capable of swimming at high Reynolds numbers had evolved, diversificatron of the new life form filled this niche as if the old adage of the horror vacui of nature was in fact the description of a strategy of evolution.
W. Wieser lnstitiit fiir Zoologie und Limnologie, UniversiGt Innsbruck, Technikerstrasse 25, A-6020 Innsbruck, Austria
Induced defenses and phenotypic plasticity Dewitt et al.‘sl recent timely treatment of the costs and limits of phenotypic plasticity includes several examples from the animal literature. I suggest that the plant literature, especially concerning inducible defenses, is also highly pertinent. The wealth of knowledge about the mechanisms by which plants with inducible defenses sense, signal and respond to environmental stimuli should provide a firm foundation to guide studies regarding costs and limits to the benefit of plasticity2. Nonetheless, induced defense in plants has rarely been studied in the context of phenotypic plasticity. For example, while individual plants or species are often qualitatively considered ‘inducible’ (plastic) or ‘not inducible’, genetic variation in inducibility (plasticity) within a species has rarely been quantified. While the benefits of induced defense have been widely studied2. costs of induced defense have received less attention3, relative to the costs of constitutive defense in plants4. Because costs of defense are assumed in theoretical models of plant defense (although their existence and magnitude are still widely debated)5, plasticity in defense expression is thought to have evolved as a cost-saving mechanism, whereby costly defense IS not expressed unless warranted by the environmente. This framework for the evolution of induced defense assumes that the ancestral state was constitutively defended (not plastic) and continuously paying production costs. In this commonly-accepted scenario, costs of plasticity
Ltd. All rights
reserved.
0169-5347/98/$19.00
should never outweigh costs of constitutive production, or its evolution would not be favored; thus, costs of plasticity in defense are currently not expected to be high and are, in turn, infrequently examined. On the other hand, if the ancestral state were considered to be undefended, plasticity costs would be expected to be higher, thus increasing the odds of their detection and the likelihood that they would be examined. Knowledge of the ancestral state is necessary in making predictions about costs and limits on the evolution of plasticity in defense and could be gained through a phylogenetic perspective of induced defense’. Lack of such knowledge has probably constrained the analysis of induced defenses in the context of phenotypic plasticity The literature on inducible defenses in plants has suggested that maintenance and production costs of induced defenses can exist (Ref. 3, but see Ref. 8). It suggests that information acquisition costs may currently be minimal, owing to the evolution of shared sensory and signaling pathways co-opted from pathways used in normal plant developmentg,lO. However, the use of shared signaling pathways could lead to a greater possibility of phenotypic error and the induction of defense out of contextll, suggesting that information reliability may limit the benefit of plasticity in defense. This possibility may have favored the evolution of the recognition of specific elicitors to signal more precisely the presence of natural enemiese. Lag-time limits can determine the effectiveness of induced defense, and are sufficient to differentiate resistant from susceptible genotypes of some plant+. Finally, the fact that many plants can induce defense to extreme levels suggest that developmental range limits may not be a limit to the benefit of plasticity12. These examples suggest that many issues regarding the type and magnitude of costs and limits to the benefits of phenotypic plasticity could be addressed in an integrated study of induced defenses in plants.
Don Cipollini Dept of Ecology and Evolution, University of Chicago, 1101East 57th Street, Chicago, IL 60637,USA References 1 Dewitt, T.J. et al. (1998) 77-81
Trends
Ecol.
Evol. 13,
2 Karban, R. and Baldwrn, I.T. (1997) induced Responses to Herbivory, University of Chicago Press 3 Baldwin, I.T. et al. (1990) Ecology71, 252-262 4 Bergelson, J. and Purrington, C. (1996) Am. Nat.
148,536-558 5 Skogsmyr,
I. and Fagerstrom,
T. (1992)
O&OS 64,
451-457 6 Karban, R. and Myers. J.H. (1989) Ecol. Syst.20,331-348 7 Doughty,P.(1995) ActaOecol.16,
Annu.
Rev.
519-524
8 Brown, D.G. (1988) Oecologia 76, 467-470 9 Staskawicz, B.J. et a/.(1995) Science268,
661-667 10 Ecker, J.R. (1995) Science 268, 667-670 11 Cipollini, D.F. (1997)
Oecologia
111.
12 Gustafson. G. and Ryan, C.A. (1976) Chem.251,7004-7010
84-90 J. Biol.
TREEuol. 13, no. 5May 1998
Tibor
Jermy
Plant Protection Institute, Hungarian Academy of Sciences, PO Box 102, H-1525 Budapest, Hungary References 1 Maynard Smith, J. and Szathmaty, The Major
Transitions
E. (1995)
in Evolution,
W.H. Freeman 2 Crick. F.H.C. (1968) J. MO/ Viol. 38, 367-379 3 Wieser. W. (1997) Trends Ecol. Evol.12, 367-370 4 Jermy,T. (1993) Entomol. Exp.Appl.66, 3-12 5 Menken, S.B.J. (1996) Entomol. Exp. Appl. 80, 297-305
6 Jacob, F. (1981)
200
Copyright
Le Jeu des Possibles, 0 1998,
Elsevier
Fayard Science
Reply from W. Wieser Tibor Jermy takes me to task for calling ecological diversification a ‘driving force’ behind the ‘major transitions in evolution’. He is right. I shouldn’t have put it this way. Ecological diversification cannot be a ‘force’ for the same reason that selection cannot exert ‘pressure’. What was implied is that each transition opened up new ecological potentials that were exploited, sometimes with extraordinary rapidity, by a new class of biological systems the members of which had become units of selection. Consider my example of large metazoans, derived from unicellular organisms, colonizing the up-to-then pristine oceanic niche in which locomotion is not seriously impeded by the viscosity of water. Once organisms capable of swimming at high Reynolds numbers had evolved, diversificatron of the new life form filled this niche as if the old adage of the horror vacui of nature was in fact the description of a strategy of evolution.
W. Wieser lnstitiit fiir Zoologie und Limnologie, UniversiGt Innsbruck, Technikerstrasse 25, A-6020 Innsbruck, Austria
Induced defenses and phenotypic plasticity Dewitt et al.‘sl recent timely treatment of the costs and limits of phenotypic plasticity includes several examples from the animal literature. I suggest that the plant literature, especially concerning inducible defenses, is also highly pertinent. The wealth of knowledge about the mechanisms by which plants with inducible defenses sense, signal and respond to environmental stimuli should provide a firm foundation to guide studies regarding costs and limits to the benefit of plasticity2. Nonetheless, induced defense in plants has rarely been studied in the context of phenotypic plasticity. For example, while individual plants or species are often qualitatively considered ‘inducible’ (plastic) or ‘not inducible’, genetic variation in inducibility (plasticity) within a species has rarely been quantified. While the benefits of induced defense have been widely studied2. costs of induced defense have received less attention3, relative to the costs of constitutive defense in plants4. Because costs of defense are assumed in theoretical models of plant defense (although their existence and magnitude are still widely debated)5, plasticity in defense expression is thought to have evolved as a cost-saving mechanism, whereby costly defense IS not expressed unless warranted by the environmente. This framework for the evolution of induced defense assumes that the ancestral state was constitutively defended (not plastic) and continuously paying production costs. In this commonly-accepted scenario, costs of plasticity
Ltd. All rights
reserved.
0169-5347/98/$19.00
should never outweigh costs of constitutive production, or its evolution would not be favored; thus, costs of plasticity in defense are currently not expected to be high and are, in turn, infrequently examined. On the other hand, if the ancestral state were considered to be undefended, plasticity costs would be expected to be higher, thus increasing the odds of their detection and the likelihood that they would be examined. Knowledge of the ancestral state is necessary in making predictions about costs and limits on the evolution of plasticity in defense and could be gained through a phylogenetic perspective of induced defense’. Lack of such knowledge has probably constrained the analysis of induced defenses in the context of phenotypic plasticity The literature on inducible defenses in plants has suggested that maintenance and production costs of induced defenses can exist (Ref. 3, but see Ref. 8). It suggests that information acquisition costs may currently be minimal, owing to the evolution of shared sensory and signaling pathways co-opted from pathways used in normal plant developmentg,lO. However, the use of shared signaling pathways could lead to a greater possibility of phenotypic error and the induction of defense out of contextll, suggesting that information reliability may limit the benefit of plasticity in defense. This possibility may have favored the evolution of the recognition of specific elicitors to signal more precisely the presence of natural enemiese. Lag-time limits can determine the effectiveness of induced defense, and are sufficient to differentiate resistant from susceptible genotypes of some plant+. Finally, the fact that many plants can induce defense to extreme levels suggest that developmental range limits may not be a limit to the benefit of plasticity12. These examples suggest that many issues regarding the type and magnitude of costs and limits to the benefits of phenotypic plasticity could be addressed in an integrated study of induced defenses in plants.
Don Cipollini Dept of Ecology and Evolution, University of Chicago, 1101East 57th Street, Chicago, IL 60637,USA References 1 Dewitt, T.J. et al. (1998) 77-81
Trends
Ecol.
Evol. 13,
2 Karban, R. and Baldwrn, I.T. (1997) induced Responses to Herbivory, University of Chicago Press 3 Baldwin, I.T. et al. (1990) Ecology71, 252-262 4 Bergelson, J. and Purrington, C. (1996) Am. Nat.
148,536-558 5 Skogsmyr,
I. and Fagerstrom,
T. (1992)
O&OS 64,
451-457 6 Karban, R. and Myers. J.H. (1989) Ecol. Syst.20,331-348 7 Doughty,P.(1995) ActaOecol.16,
Annu.
Rev.
519-524
8 Brown, D.G. (1988) Oecologia 76, 467-470 9 Staskawicz, B.J. et a/.(1995) Science268,
661-667 10 Ecker, J.R. (1995) Science 268, 667-670 11 Cipollini, D.F. (1997)
Oecologia
111.
12 Gustafson. G. and Ryan, C.A. (1976) Chem.251,7004-7010
84-90 J. Biol.
TREEuol. 13, no. 5May 1998