- Email: [email protected]
Evolution of resistance and virulence in plant-herbivore and plant-pathogen interactions
TREE vol. 7, no. 4, April
8 Jacobs, L.L., Flynn, L.J. and Downs, W.R. (1989) in Papers on Fossil Rodents in Honor of Albert Elmer Wood (Black, CC. and Dawson. M.R., eds), pp. 157-177, Natural History Museum of Los Angeles County, Sciences Ser. 33 9 Pascale, E., Valle, E. and Furano, A.V. ( I9901 Proc. Nat/ Acad. Sci. USA 87, 948 l-9485 IO de long. W.W. (19851 in Evolutionary Relationships among Rodents (Luckett,
W.P. and Hartenberger, I-L., edsl, pp. 2 I l-226, Plenum Press I I Aguilar, J-P. et a/. ( 1978) C. R. Acad. Sci. Paris 287 (Ser. D), 439-442 12 Chaline, I. and Graf, J-D. (19881 1. Mammal. 69, 22-33 I3 Stein, B.R. (1987) 2. SJugetierkd. 52, 140-156 14 Brownell, E. 119831 Evolution 37, 1034-1051 15 Catzeflis, F.M., Sheldon, F.H., Ahlquist, I.E. and Sibley, CC. ( 1987) Mol. Biol. Evol. 4. 242-253 16 Tong, H. (1989) Mem. Sot. Geol. Fr. 155, I-120 I7 lacobs, L.L ( 1978) Mus. North. Ariz. Bull
52, I-103 I8 Catzeflis, F.M. II9901 in Evolution Subterranean and Molecular
29 Brown, W.H., Prager, E.M., Wang, A. and Wilson, A.C. ( 19821/. Mol. Evol. 18, 225-239 30 Schiiller, C., Neuteboom, B., Wiibbels, G.H., Beintema, 1.1.and Nevo, E. (1989)
of Mammals at the Organismal Levels (Nevo. E. and Reig.
O.A.. edsl. pp. 317-345, Alan R. Liss I9 Denys, C. ( 1990) Paleontographica
Biol. Abt.
A
210,79-91 20 Reig. O.A. t 1987) Fieldiana Zoo/. 39, 347-400 21 Baskin, ].A. 11986) Contrib. Geol. Univ. Wyoming, Spec. Pap. 3, 287-303 22 Hand, S. (19841 in Vertebrate Zoogeography and Evolution in Australasia
(Archer, M. and Clayton, C., eds), pp. 905-9 12. Hesperian Press 23 Jaeger, j-l., Tong, H. and Denys, C. ( 1986) C. R. Acad. Sci. Paris 302 (Ser. 21, 9 17-922 24 Laird, C.D., McConaughy, B.L. and McCarthy, BJ. (19691 Nature 224, 149-154 25 Britten, R.I. (I9861 Science 231. 1393-1398 26 Graur, D., Shuali, Y. and Li, W-H. (1989) 1. Mol. Evol. 28, 279-285 27 Wilson, A.C. et al. I 19851 Biol. /. Linn. Sot. 26, 375-400 28 Harrison, R.G. (1989) Trends 4,6-II
Eco/. Evol.
Evolutionof Resistanceand Virulencein Plant-Herbivoreand Plant-PathogenInteractions Robert J. Marquis and Helen Miller Alexander HerGiwres and pathogens often attack or infect the same plant parts, and the same plant traits can affect the likelihood and degree of damage. Research on plant her6ivore and plant-pathogen interactions in natural systems have, however, proceeded largely independently of each other. Our understanding of both types of plant-enemy interaction would be enhanced by greater exposure of researchers to developments in both disciplines and by more studies of interudions between pathogen and herbivore species associated with the same hosts. interactions beEvolutionary tween plants and their natural enemies are mediated by the ability of the plant enemy to attack its host, and the ability of the host plant to resist such attack. The driving forces behind evolutionary changes in
Robert Marquis is at the Dept of Biology, University of Missouri at St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63 I2 l-4499, USA; Helen Alexander is at the Depts of Botany and Systematics & Ecology, University of Kansas, Lawrence, KS66045-2106,USA.
126
1992
virulence and resistance traits are reciprocal impacts on plant and enemy fitness due to their interactions. Most of our information on these interactions comes from agriculture, where heritable differences in crop susceptibility have been manipulated through breeding to improve pest and disease resistance. Recently, however, there have been abundant studies of plant-herbivore and plant-pathogen interactions in natural plant communities. Here, we compare the research goals of both disciplines with regard to the evolution of traits that affect these interactions. Herbivores and pathogens are likely to interact with each other, as well as individually with their host plant. We hope that future research will avoid the problem summarized by Agrios’: ‘The tendency for the pathologist to attribute all the damage [in plants! to the fungus and to overlook the role of the insect appears to be equaled by the tendency of the entomologist to attribute everything to the insect
Chem.
Hoppe-Seyler
370, 583-589
II Bonhomme, F., Iskandar, D., Thaler, L. and Petter, F. ( 19851 in Evolutionary Relationships among Rodents (Luckett, W.P. and Hartenberger, I-L., eds), pp. 671-684, Plenum Press 32 Easteal, S. (1988) Proc. Nat/ Acad. Sci. USA 85, 7622-7626 33 Li, W-H., Couy,
M., Sharp, P.M., O’Huigin, C. and Yang, Y-W. (1990) Proc. Nat/ Acad.
Sci. USA 87, 6703-6707 34 Scherer, S. ( 1989) Mol. Biol. Evol. 6, 436-44 I 35 Musser, C.G. II981 1Bull. Am. Mus. Nat Hist 168, 255-334 36 Musser, G.G. and Newcomb, C. (1983) Bull. Am. Mus. Nat. Hist. 174. 327-598 37 Musser, G.G. 11982) Bull. Am. Mus. Nat Hist. 174, l-95 38 Voss, R.S. (19881 Bull. Am. Mus. Nat. Hist. 188, 259-493 39 Qumsiyeh, M.B. and Chesser, R.K. ( 19881 Biochem. Syst. Ecol. 16, 89-103
and to overlook the fact that insect invaders of plants are always, and without any exception, accompanied or followed by fungi and bacteria’. Insects and fungi, which are the focus of this article, span a continuum in terms of their mode of attack. Feeding by insects can either be from the exterior or from the interior, while fungi must invade host tissue directly through the cuticle, or through a wound or stoma. Except for a few windblown taxa, insects actively search for their hosts by following either visual or olfactory cues or both. In contrast, fungal pathogens often are moved passively by wind, water or animal vectors, but they can spread actively through soil. Life cycles are diverse in both groups, with asexual reproduction more prevalent in fungi. To simplify discussion, we use the term virulence to referto both the relative ability of pathogens to infect their hosts and the relative ability of herbivores to feed on their hosts. Evolution of insect herbivore virulence and plant resistance Recent interest in natural plantherbivore interactions was stimulated in part by the hypothesis2, followed by the general acceptance-, that plant allelochemicals diversified as a result of evol0
1992.
Elsever
Science
Publishers
Ltd (UK1
TREE vol. 7, no. 4, April
1992
utionary interactions with biotic particularly herbivores. agents, Such coevolutionary spiraling was proposed to lead to speciation in both the herbivores and their host plants4. Since these initial proposals, there has been no detailed examination of coevolution between populations of plants and herbivores, although certain components of the coevolutionary process have been well documented. For example, the impact of herbivores on plant fitness has been found to be almost universally negative7. Similarly, variation in host-plant traits can have a selective impact on the insects that feed on thema. For plants, the biochemical and physical traits that account for resistance have been determined for many species3. General patterns of interspecific secondary compound distribution have been described5 and placed in the general context of life history theory5rb. For insects, the enzymatic detoxification systems and morphological traits that allow herbivores to utilize their host plants have been analysed in detail for a few systems9. Both diet breadth and phylogeny appear to influence traits involved in hostplant utilization9. Although plant chemical and physical traits that directly affect herbivore feeding have been championed as the main factors determining damage, plant traits that influence predator and parasite attack on herbivores must also be considered’O. These tritrophic interactions impose evolutionary constraintson both herbivoreand plant, because plant traits influence not only the herbivore directly but also the probability of predation and parasitism on herbivores. The relative importance for plant fitness of direct interactions between the plant and its herbivores versus indirect interactions through three trophic levels needs to be clarified. Regardless of its mechanistic basis, several studies have shown that intrapopulational variation in plant resistance traits has a genetic basis”. From the insect side, genetic variation underlying the ability to utilize different hosts within the same and different plant species has been demonstrated12,‘3, but has not been related to variation in
actual traits that influence such virulence. The time scale over which natural plant populations respond evolutionarily to insect attack, and vice versa, in the face of other selection pressures is not known. One such additional selection pressure could be the influence of pathogens. Evolution of fungal pathogen virulence and plant resistance As with studies of plant-herbivore interactions, the possibility of coevolution between plants and pathogens has been an important theme. In contrast to Ehrlich and Raven’s original theory conceming plant-herbivore coevolution4, coevolution between plants and pathogens was originally postulated without speciation; the emphasis instead has been on reciprocal selection through ‘gene-for-gene interactions’ (control of resistance and virulence by genes acting in complimentary fashion)‘4. The ‘gene-for-gene’ paradigm, plus a long history of discovering useful resistance genes in wild crop progenitors, led to examinations of the resistance and virulence structure of natural plant and pathogen populations. Variation in resistance to several foliar pathogens has been shown to be controlled by one or a few genes, although polygenically based variation also has been reported’5,‘6. Studies of pathogen virulence are less common in natural systems, but simple inheritance has been found15. Because of the relative ease of storing fungal strains and performing inoculations, researchers have been able to document resistance and virulence variation for many populations in some systems. This large-scale view has suggested that diversity in resistance and virulence structure may be greater in areas with higher disease levels (presumably stronger selection)‘5. Similar studies with insect herbivores have demonstrated genetic variation for host use within insect populations I*, but such studies are often less practicable because of the problem of storing and testing insects. Despite the impressive data on resistance and virulence structure in natural systems, we have little knowledge at the biochemical or
molecular level of the traits that contribute to this variation. For example, although the role of allelochemicals in plant pathology has been studiedj7, this research has rarely been combined with studies of resistance and virulence in natural populations. Further, data on the ecological consequences of resistance are often lacking: that is, how does the pathogen affect plant fitness and what is the selective effect of resistance? Most studies of pathogen effects on plant survival and reproduction are correlative, comparing demographic characteristics of naturally infected versus healthy individuals. Experimental approaches that remove or add pathogens (i.e. fungicide or inoculation treatments, respectively) are being promoted I6, but are uncommon in studies of natural populations The available data do suggest, however, that fungi have a variety of effects, ranging from the lethal effects of seed and seedling pathogens, to reduced growth, competitive ability or reproduction of plants with foliar pathogens, to the potential for mutualism with systemic fungi such as the endophytes’5,‘6,‘8. In plant-herbivore studies, much work has been done on how resistance factors affect the insect’s attraction to the plant, its ability to digest plant tissue, and the diet’s effect on insect growth and reproduction9. Similar detail on the effects of host plants on pathogen biology in natural systems is lacking. The passive dispersal of many pathogens reduces the need for ‘host-plant choice’ experiments, but more information is needed on production and dispersal of spores and on whether pathogens compete for resources within a plant. The basic problem involves defining and quantifying characteristics of the fungal ‘individual’19. Further, researchers studying plant-pathogen interactions in nature often lack a plant pathology background, leading to greater emphasis on the plant side of the interaction. Integration of disciplines and new directions The similarity in the effects of insect herbivores and fungal pathogens on plant fitness has long been noted*O. Thus, although these 127
TREE vol. 7, no. 4, April
taxa differ in the mechanisms by which they obtain energy from plants, they potentially have similar and interactive ecological and evolutionary effects on plant populations. To understand how traits that have been attributed to evolutionary interactions between plants and their enemies evolve, we must consider at least the following areas. ( I ) Biologicalbasis for resistanceand virulence Knowledge of the traits responsible for variation in resistance and virulence is essential to understand the constraints on their evolution in response to selection. Studies of plant-pathogen interactions in natural systems have thus far emphasized patterns of variation in resistance and virulence within and among populations and their mode of inheritance, rather than examination of the actual traits (e.g. phytoalexin production, cellulase activity) that might contribute to resistance and virulence. Researchers of plant-herbivore systems have emphasized the mechanisms of plant resistance, but to the relative neglect of virulence traits in the herbivore. Where both pathogens and herbivores are important, we must consider how the traits of one participant mediate the interactions of all three taxa (e.g. plant traits affecting resistance to both herbivores and pathogens2’). Such a comprehensive approach may allow us to find predictable suites of traits, associated with plant life history, that provide resistance against herbivore and pathogen species, in a manner already proposed for defenses against herbivores alone5,6. (2) Natural enemies as selectiveagents for plant traits, and plants as selective agents for enemy traits For practical reasons, most research has stressed ‘one-on-one’ interactions, i.e. the effect of one plant species on one enemy species, and vice versa. From the plant point of view, future work should stress how the combined community of plant enemies interacts to alter plant survival and reproduction22. Relevant questions include how the presence of one enemy species alters the likelihood or success of infection or attack by 128
others, and whether the net effect of many species on plant fitness is additive or nonadditive22. From the plant enemy point of view, the presence of other herbivores for damage they cause) may be important, either because of direct usurpation of the resource or because of a change in resource quality through induction. Even less is known about herbivore-pathogen interactions. Most work to date has been on symbiotic relationships in which a fungus and insect interact mutualistically to overcome host defenses23, or cases in which endophytic fungi provide protection for the plants against their herbivores’s. Investigation of less tightly evolved natural systems is limited, but suggests that the presence of one plant enemy can either facilitate or inhibit the ability of other plant enemies to attack the shared host plant’,24; the role of herbivores as disease vectors’ is a prime example. Finally, because plant enemy population levels and the damage they cause can vary greatly among years at the same site, as well as across sites within the same year7, efforts should be made to study temporal and geographic variation in interactions between plants and their community of enemies.
(3) Inter- and intrapopulation variation in resistanceand virulence To determine the potential for response to selection, we must ascertain the extent of genetic variation for traits that affect the interaction between plant and plant enemy. In plant-herbivore systems, we are just beginning to couple studies of the genetic basis of plant resistance traits with their contribution to fitness in the field25. Studies of the degree to which utilization of different host species varies within populations of polyphagous insects suggest that local adaptation to a particular host species is possiblei2. However, the actual traits that account for variation in fitness are unknown. As mentioned previously, studies in plantof genetic variation pathogen systems have been relatively simple, because of the relative technical ease of working with microorganisms. However, to interpret studies of disease resist-
7992
ante structure in plant populations, we need more rigorous measurements of the effect of disease and of resistance genes on plant fitness. Inheritance patterns of host resistance and enemy virulence also require attention given the controversy regarding the general applicability of the genefor-gene model of host-parasite interactions26. Besides quantifying resistance, we must define explicitly the environmental factors that influence attack. By doing so, we can determine both the role of environmental factors as selective forces (and thus their relative importance versus enemy attack), and the degree to which the environment interacts with genotype to determine plant and plant enemy fitness. (4) Fitness costs of plant resistance and fitness costs of enemies’ virulence Models of genetic interactions between host plants and their enemies assume that potential evolutionary pathways are limited by the ‘costs’ of resistance or virulence27, but experimental data are generally lacking. At the phenotypic level, the cost of resistance in plants is the decrease in fitness due to diversion of resources away from growth and reproduction. Costs measured at the genotypic level are those due to negative genetic correlations between the magnitude of a resistance trait(s) and fitness. Estimates of the cost of plant resistance to either herbivore or pathogens separately will be misleading if such traits provide protection against both sets of enemies2’. The phenotypic cost of virulence in plant enemies is focused on whether enemies that utilize a wide range of hosts and/or genotypes have lower fitness than those with a narrower host range. The technical ease of working with fungi has led to several studies of this phenomenon’9. In contrast, tradeoffs in ability of insects to attack have been tested primarily across plant species rather than across different genotypes of the same plant species’2. The costs of virulence due to negative genetic correlations need to be investigated further, especially for variation in ability to use different individuals within a host species.
TREE vol. 7, no. 4, April 1992
(5) Pkylogeny of traits that confer resistance and virulence By identifying traits that affect plant-enemy interactions (e.g. particular plant secondary chemicals), we can develop hypotheses about their phylogenetic histories. This will allow us to determine how frequently such traits are lost and gained, the degree to which phylogenetic patterns are consistent with the hypothesis of coevolution, and whether certain evolutionary pathways are more likely than othersZ6, perhaps because of differential costs of resistance or virulence associated with different pathways. For example, do we see the independent evolution of resistance characters in many lineages, or are certain resistance traits ancestral, and thus their appearance throughout a lineage simply a reflection of historical development? Analyses of Ehrlich and Raven’s hypothesis4 of ‘escape and radiation’ coevolution have led to varied results, depending on the system studied and systematic interpretation used28. A similar emphasis on macroevolutionary trends is generally lacking in studies of plant-pathogen interactions in natural systems. Because the traits under consideration (e.g. secondary compounds) are likely to respond in evolutionary time to both herbivores and pathogens, ideally both sets of plant enemies should be considered in interpretation of patterns. An integratedapproach Clearly, approaches to the study of plant-herbivore and plantpathogen interactions often differ. These differences result from historical research trends (for example, the early emphasis on secondary chemicals and herbivores) and the practicalities of working with different organisms. Because the two sets of interactions are similiar, researchers can gain insights by borrowing approaches commonly used in the other discipline. However, we should not ignore the possibility that herbivores and pathogens may differ fundamentally in their evolutionary interactions with their plant hosts. For example, does the prevalence of asexual reproduction in many pathogenic fungi mean that coevolution could
proceed in a different way than expected with herbivorous insects? It is not a trivial task to adopt a more comprehensive view of one’s study system if it includes numerous herbivore and pathogen species. In order to study multiple species, the number of experimental treatments and field measurements required increases dramatically, and the potential for complex interactions makes data interpretation difficult. However, our understanding of the evolution of certain traits will be limited as long as we ignore the role of herbivores in plant-pathogen interactions and vice versa. Some systems, in which two interactors significantly affect the third, have already demanded an analysis of multiple herbivores and pathogens ‘**23.Results of these studies suggest that an integrative approach can be insightful, and worthy of greater attention in the future. Even if one’s research remains focused on a herbivore or pathogen, the parallels between the fields require a broader crossfertilization of ideas than currently exists. Acknowledgements We thank j. Burdon. I. Frazee, C. Hochwender, C. Israel, C. Kelly, M. Parker, N. Schellhorn, E. Simms, K. Stowe, E. Wienerand three anonymous reviewers for their comments on earlier drafts of this paper.
References
of
I Agrios. G.N. ( 1980) in Vectors Plant Pathogens (Harris, K.F. and Maramorosch. K., eds), pp. 293-324, Academic Press 2 Fraenkel, G.S. ( 1959) Science 129. 1466-1470 3 Rosenthal, G.A. and Janzen, D.H.. eds ( I9791 Herbivores: Their Interactions with Plant Secondary Metabolites. Academic Press 4 Ehrlich, P.R. and Raven, P.H. ( 1964) Evolution 18, 586-608 5 Feeny, P.P. ( 1976) Recent Adv. Phytochem. 10. I-40 6 Coley, P.D., Bryant, I.P. and Chapin, F.S., Ill
( 1985) Science 230.895-899 7 Marquis, RJ. in Plant Resistance: Ecology, Evolution, and Genetics (Fritz, R.S. and Simms, E.L.. eds), University of Chicago Press (in press) 8 Larrson, S., Bjorkman, C. and Gref, R. ( 19861 Oecologia 70, 77-84 9 Lindroth, R.L. t 1991) in Insect-Plant (Vol. Ill) (Bernays, E., ed.1, Interactions pp. i-34, CRC Press IO Bernays, E. and Graham, M. (1988) Ecology 69,886-892 II Kennedy, C.G. and Barbour, J.D. in P/ant Resistance: Ecology. Evolution, and (Fritz, R.S. and Simms, E.L., eds), Genetics University of Chicago Press (in press) I2 Via, S. II991 I Evolution 45, 827-852 I3 Wilhoit, L. in P/ant Resistance: Ecology, (Fritz, R.S. and Evolution, and Genetics Simms, E.L., eds), University of Chicago Press (in press1 I4 Mode, C.I. 11958) Evolution 12, 158-165 I5 Burdon, 1.1. (I9871 Diseases and P/ant Population Biology, Cambridge University Press I6 Alexander, H.M. in P/ant Resistance: Ecology, Evolution, and Genetics IFritz, R.S. and Simms, E.L., edsl, University of Chicago Press lin press) I7 Goodman, R.N., Kiraly, Z. and Wood, K.R. 11986) The Biochemistry and Physiology of P/ant Disease, University of Missouri Press I8 Clay, K. (19881 in Co-evolution of fungi with Plants and Animals (Hawksworth, D.L. and Pirozynski, K., eds), pp. 79-105, Academic Press I9 Antonovics, I. and Alexander, H.M. II9891 Genetics, in Plant Disease Epidemiology, Resistance, and Management (Vol. 21 (Leonard, K.J. and Fry, W.E., edsl, pp. 185-2 14, McGraw-Hill 20 Harper, J.L. (19771 Population Biology of P/ants, Academic Press 21 Krischik, V.A., Goth, R.W. and Barbosa, P. ( I99 I I Oecologia 85, 562-57 I 22 Linhart, Y.B. ( 1991 I Trends Eco/. Eva/. 6. 392-396 23 Wilding, N., Collins, N.M., Hammond, P.M. and Webber, I.F. I19891 Insect-Plant Interactions, Academic Press 24 de Nooij, M.P. (1988) Oikos 52, 51-58 25 Berenbaum, M.R., Zangerl, A.R. and Nitao, 1.K. (1986) Evolution 40, 1215-1228 26 Barrett, 1. (1985) in Ecology and Genetics of Host-Parasite interactions (Rollinson, D. and Anderson, R.M., eds), pp. 215-225, Academic Press 27 Simms, E.L. and Fritz, R.S. 11990) Trends Ecol. Evol. 5, 356-360 28 Mitter, C.M., Farrell, B. and Futuyma, D.J. II99 I I Trends Ecol. Eva/. 6, 290-293
8 Jacobs, L.L., Flynn, L.J. and Downs, W.R. (1989) in Papers on Fossil Rodents in Honor of Albert Elmer Wood (Black, CC. and Dawson. M.R., eds), pp. 157-177, Natural History Museum of Los Angeles County, Sciences Ser. 33 9 Pascale, E., Valle, E. and Furano, A.V. ( I9901 Proc. Nat/ Acad. Sci. USA 87, 948 l-9485 IO de long. W.W. (19851 in Evolutionary Relationships among Rodents (Luckett,
W.P. and Hartenberger, I-L., edsl, pp. 2 I l-226, Plenum Press I I Aguilar, J-P. et a/. ( 1978) C. R. Acad. Sci. Paris 287 (Ser. D), 439-442 12 Chaline, I. and Graf, J-D. (19881 1. Mammal. 69, 22-33 I3 Stein, B.R. (1987) 2. SJugetierkd. 52, 140-156 14 Brownell, E. 119831 Evolution 37, 1034-1051 15 Catzeflis, F.M., Sheldon, F.H., Ahlquist, I.E. and Sibley, CC. ( 1987) Mol. Biol. Evol. 4. 242-253 16 Tong, H. (1989) Mem. Sot. Geol. Fr. 155, I-120 I7 lacobs, L.L ( 1978) Mus. North. Ariz. Bull
52, I-103 I8 Catzeflis, F.M. II9901 in Evolution Subterranean and Molecular
29 Brown, W.H., Prager, E.M., Wang, A. and Wilson, A.C. ( 19821/. Mol. Evol. 18, 225-239 30 Schiiller, C., Neuteboom, B., Wiibbels, G.H., Beintema, 1.1.and Nevo, E. (1989)
of Mammals at the Organismal Levels (Nevo. E. and Reig.
O.A.. edsl. pp. 317-345, Alan R. Liss I9 Denys, C. ( 1990) Paleontographica
Biol. Abt.
A
210,79-91 20 Reig. O.A. t 1987) Fieldiana Zoo/. 39, 347-400 21 Baskin, ].A. 11986) Contrib. Geol. Univ. Wyoming, Spec. Pap. 3, 287-303 22 Hand, S. (19841 in Vertebrate Zoogeography and Evolution in Australasia
(Archer, M. and Clayton, C., eds), pp. 905-9 12. Hesperian Press 23 Jaeger, j-l., Tong, H. and Denys, C. ( 1986) C. R. Acad. Sci. Paris 302 (Ser. 21, 9 17-922 24 Laird, C.D., McConaughy, B.L. and McCarthy, BJ. (19691 Nature 224, 149-154 25 Britten, R.I. (I9861 Science 231. 1393-1398 26 Graur, D., Shuali, Y. and Li, W-H. (1989) 1. Mol. Evol. 28, 279-285 27 Wilson, A.C. et al. I 19851 Biol. /. Linn. Sot. 26, 375-400 28 Harrison, R.G. (1989) Trends 4,6-II
Eco/. Evol.
Evolutionof Resistanceand Virulencein Plant-Herbivoreand Plant-PathogenInteractions Robert J. Marquis and Helen Miller Alexander HerGiwres and pathogens often attack or infect the same plant parts, and the same plant traits can affect the likelihood and degree of damage. Research on plant her6ivore and plant-pathogen interactions in natural systems have, however, proceeded largely independently of each other. Our understanding of both types of plant-enemy interaction would be enhanced by greater exposure of researchers to developments in both disciplines and by more studies of interudions between pathogen and herbivore species associated with the same hosts. interactions beEvolutionary tween plants and their natural enemies are mediated by the ability of the plant enemy to attack its host, and the ability of the host plant to resist such attack. The driving forces behind evolutionary changes in
Robert Marquis is at the Dept of Biology, University of Missouri at St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63 I2 l-4499, USA; Helen Alexander is at the Depts of Botany and Systematics & Ecology, University of Kansas, Lawrence, KS66045-2106,USA.
126
1992
virulence and resistance traits are reciprocal impacts on plant and enemy fitness due to their interactions. Most of our information on these interactions comes from agriculture, where heritable differences in crop susceptibility have been manipulated through breeding to improve pest and disease resistance. Recently, however, there have been abundant studies of plant-herbivore and plant-pathogen interactions in natural plant communities. Here, we compare the research goals of both disciplines with regard to the evolution of traits that affect these interactions. Herbivores and pathogens are likely to interact with each other, as well as individually with their host plant. We hope that future research will avoid the problem summarized by Agrios’: ‘The tendency for the pathologist to attribute all the damage [in plants! to the fungus and to overlook the role of the insect appears to be equaled by the tendency of the entomologist to attribute everything to the insect
Chem.
Hoppe-Seyler
370, 583-589
II Bonhomme, F., Iskandar, D., Thaler, L. and Petter, F. ( 19851 in Evolutionary Relationships among Rodents (Luckett, W.P. and Hartenberger, I-L., eds), pp. 671-684, Plenum Press 32 Easteal, S. (1988) Proc. Nat/ Acad. Sci. USA 85, 7622-7626 33 Li, W-H., Couy,
M., Sharp, P.M., O’Huigin, C. and Yang, Y-W. (1990) Proc. Nat/ Acad.
Sci. USA 87, 6703-6707 34 Scherer, S. ( 1989) Mol. Biol. Evol. 6, 436-44 I 35 Musser, C.G. II981 1Bull. Am. Mus. Nat Hist 168, 255-334 36 Musser, G.G. and Newcomb, C. (1983) Bull. Am. Mus. Nat. Hist. 174. 327-598 37 Musser, G.G. 11982) Bull. Am. Mus. Nat Hist. 174, l-95 38 Voss, R.S. (19881 Bull. Am. Mus. Nat. Hist. 188, 259-493 39 Qumsiyeh, M.B. and Chesser, R.K. ( 19881 Biochem. Syst. Ecol. 16, 89-103
and to overlook the fact that insect invaders of plants are always, and without any exception, accompanied or followed by fungi and bacteria’. Insects and fungi, which are the focus of this article, span a continuum in terms of their mode of attack. Feeding by insects can either be from the exterior or from the interior, while fungi must invade host tissue directly through the cuticle, or through a wound or stoma. Except for a few windblown taxa, insects actively search for their hosts by following either visual or olfactory cues or both. In contrast, fungal pathogens often are moved passively by wind, water or animal vectors, but they can spread actively through soil. Life cycles are diverse in both groups, with asexual reproduction more prevalent in fungi. To simplify discussion, we use the term virulence to referto both the relative ability of pathogens to infect their hosts and the relative ability of herbivores to feed on their hosts. Evolution of insect herbivore virulence and plant resistance Recent interest in natural plantherbivore interactions was stimulated in part by the hypothesis2, followed by the general acceptance-, that plant allelochemicals diversified as a result of evol0
1992.
Elsever
Science
Publishers
Ltd (UK1
TREE vol. 7, no. 4, April
1992
utionary interactions with biotic particularly herbivores. agents, Such coevolutionary spiraling was proposed to lead to speciation in both the herbivores and their host plants4. Since these initial proposals, there has been no detailed examination of coevolution between populations of plants and herbivores, although certain components of the coevolutionary process have been well documented. For example, the impact of herbivores on plant fitness has been found to be almost universally negative7. Similarly, variation in host-plant traits can have a selective impact on the insects that feed on thema. For plants, the biochemical and physical traits that account for resistance have been determined for many species3. General patterns of interspecific secondary compound distribution have been described5 and placed in the general context of life history theory5rb. For insects, the enzymatic detoxification systems and morphological traits that allow herbivores to utilize their host plants have been analysed in detail for a few systems9. Both diet breadth and phylogeny appear to influence traits involved in hostplant utilization9. Although plant chemical and physical traits that directly affect herbivore feeding have been championed as the main factors determining damage, plant traits that influence predator and parasite attack on herbivores must also be considered’O. These tritrophic interactions impose evolutionary constraintson both herbivoreand plant, because plant traits influence not only the herbivore directly but also the probability of predation and parasitism on herbivores. The relative importance for plant fitness of direct interactions between the plant and its herbivores versus indirect interactions through three trophic levels needs to be clarified. Regardless of its mechanistic basis, several studies have shown that intrapopulational variation in plant resistance traits has a genetic basis”. From the insect side, genetic variation underlying the ability to utilize different hosts within the same and different plant species has been demonstrated12,‘3, but has not been related to variation in
actual traits that influence such virulence. The time scale over which natural plant populations respond evolutionarily to insect attack, and vice versa, in the face of other selection pressures is not known. One such additional selection pressure could be the influence of pathogens. Evolution of fungal pathogen virulence and plant resistance As with studies of plant-herbivore interactions, the possibility of coevolution between plants and pathogens has been an important theme. In contrast to Ehrlich and Raven’s original theory conceming plant-herbivore coevolution4, coevolution between plants and pathogens was originally postulated without speciation; the emphasis instead has been on reciprocal selection through ‘gene-for-gene interactions’ (control of resistance and virulence by genes acting in complimentary fashion)‘4. The ‘gene-for-gene’ paradigm, plus a long history of discovering useful resistance genes in wild crop progenitors, led to examinations of the resistance and virulence structure of natural plant and pathogen populations. Variation in resistance to several foliar pathogens has been shown to be controlled by one or a few genes, although polygenically based variation also has been reported’5,‘6. Studies of pathogen virulence are less common in natural systems, but simple inheritance has been found15. Because of the relative ease of storing fungal strains and performing inoculations, researchers have been able to document resistance and virulence variation for many populations in some systems. This large-scale view has suggested that diversity in resistance and virulence structure may be greater in areas with higher disease levels (presumably stronger selection)‘5. Similar studies with insect herbivores have demonstrated genetic variation for host use within insect populations I*, but such studies are often less practicable because of the problem of storing and testing insects. Despite the impressive data on resistance and virulence structure in natural systems, we have little knowledge at the biochemical or
molecular level of the traits that contribute to this variation. For example, although the role of allelochemicals in plant pathology has been studiedj7, this research has rarely been combined with studies of resistance and virulence in natural populations. Further, data on the ecological consequences of resistance are often lacking: that is, how does the pathogen affect plant fitness and what is the selective effect of resistance? Most studies of pathogen effects on plant survival and reproduction are correlative, comparing demographic characteristics of naturally infected versus healthy individuals. Experimental approaches that remove or add pathogens (i.e. fungicide or inoculation treatments, respectively) are being promoted I6, but are uncommon in studies of natural populations The available data do suggest, however, that fungi have a variety of effects, ranging from the lethal effects of seed and seedling pathogens, to reduced growth, competitive ability or reproduction of plants with foliar pathogens, to the potential for mutualism with systemic fungi such as the endophytes’5,‘6,‘8. In plant-herbivore studies, much work has been done on how resistance factors affect the insect’s attraction to the plant, its ability to digest plant tissue, and the diet’s effect on insect growth and reproduction9. Similar detail on the effects of host plants on pathogen biology in natural systems is lacking. The passive dispersal of many pathogens reduces the need for ‘host-plant choice’ experiments, but more information is needed on production and dispersal of spores and on whether pathogens compete for resources within a plant. The basic problem involves defining and quantifying characteristics of the fungal ‘individual’19. Further, researchers studying plant-pathogen interactions in nature often lack a plant pathology background, leading to greater emphasis on the plant side of the interaction. Integration of disciplines and new directions The similarity in the effects of insect herbivores and fungal pathogens on plant fitness has long been noted*O. Thus, although these 127
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taxa differ in the mechanisms by which they obtain energy from plants, they potentially have similar and interactive ecological and evolutionary effects on plant populations. To understand how traits that have been attributed to evolutionary interactions between plants and their enemies evolve, we must consider at least the following areas. ( I ) Biologicalbasis for resistanceand virulence Knowledge of the traits responsible for variation in resistance and virulence is essential to understand the constraints on their evolution in response to selection. Studies of plant-pathogen interactions in natural systems have thus far emphasized patterns of variation in resistance and virulence within and among populations and their mode of inheritance, rather than examination of the actual traits (e.g. phytoalexin production, cellulase activity) that might contribute to resistance and virulence. Researchers of plant-herbivore systems have emphasized the mechanisms of plant resistance, but to the relative neglect of virulence traits in the herbivore. Where both pathogens and herbivores are important, we must consider how the traits of one participant mediate the interactions of all three taxa (e.g. plant traits affecting resistance to both herbivores and pathogens2’). Such a comprehensive approach may allow us to find predictable suites of traits, associated with plant life history, that provide resistance against herbivore and pathogen species, in a manner already proposed for defenses against herbivores alone5,6. (2) Natural enemies as selectiveagents for plant traits, and plants as selective agents for enemy traits For practical reasons, most research has stressed ‘one-on-one’ interactions, i.e. the effect of one plant species on one enemy species, and vice versa. From the plant point of view, future work should stress how the combined community of plant enemies interacts to alter plant survival and reproduction22. Relevant questions include how the presence of one enemy species alters the likelihood or success of infection or attack by 128
others, and whether the net effect of many species on plant fitness is additive or nonadditive22. From the plant enemy point of view, the presence of other herbivores for damage they cause) may be important, either because of direct usurpation of the resource or because of a change in resource quality through induction. Even less is known about herbivore-pathogen interactions. Most work to date has been on symbiotic relationships in which a fungus and insect interact mutualistically to overcome host defenses23, or cases in which endophytic fungi provide protection for the plants against their herbivores’s. Investigation of less tightly evolved natural systems is limited, but suggests that the presence of one plant enemy can either facilitate or inhibit the ability of other plant enemies to attack the shared host plant’,24; the role of herbivores as disease vectors’ is a prime example. Finally, because plant enemy population levels and the damage they cause can vary greatly among years at the same site, as well as across sites within the same year7, efforts should be made to study temporal and geographic variation in interactions between plants and their community of enemies.
(3) Inter- and intrapopulation variation in resistanceand virulence To determine the potential for response to selection, we must ascertain the extent of genetic variation for traits that affect the interaction between plant and plant enemy. In plant-herbivore systems, we are just beginning to couple studies of the genetic basis of plant resistance traits with their contribution to fitness in the field25. Studies of the degree to which utilization of different host species varies within populations of polyphagous insects suggest that local adaptation to a particular host species is possiblei2. However, the actual traits that account for variation in fitness are unknown. As mentioned previously, studies in plantof genetic variation pathogen systems have been relatively simple, because of the relative technical ease of working with microorganisms. However, to interpret studies of disease resist-
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ante structure in plant populations, we need more rigorous measurements of the effect of disease and of resistance genes on plant fitness. Inheritance patterns of host resistance and enemy virulence also require attention given the controversy regarding the general applicability of the genefor-gene model of host-parasite interactions26. Besides quantifying resistance, we must define explicitly the environmental factors that influence attack. By doing so, we can determine both the role of environmental factors as selective forces (and thus their relative importance versus enemy attack), and the degree to which the environment interacts with genotype to determine plant and plant enemy fitness. (4) Fitness costs of plant resistance and fitness costs of enemies’ virulence Models of genetic interactions between host plants and their enemies assume that potential evolutionary pathways are limited by the ‘costs’ of resistance or virulence27, but experimental data are generally lacking. At the phenotypic level, the cost of resistance in plants is the decrease in fitness due to diversion of resources away from growth and reproduction. Costs measured at the genotypic level are those due to negative genetic correlations between the magnitude of a resistance trait(s) and fitness. Estimates of the cost of plant resistance to either herbivore or pathogens separately will be misleading if such traits provide protection against both sets of enemies2’. The phenotypic cost of virulence in plant enemies is focused on whether enemies that utilize a wide range of hosts and/or genotypes have lower fitness than those with a narrower host range. The technical ease of working with fungi has led to several studies of this phenomenon’9. In contrast, tradeoffs in ability of insects to attack have been tested primarily across plant species rather than across different genotypes of the same plant species’2. The costs of virulence due to negative genetic correlations need to be investigated further, especially for variation in ability to use different individuals within a host species.
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(5) Pkylogeny of traits that confer resistance and virulence By identifying traits that affect plant-enemy interactions (e.g. particular plant secondary chemicals), we can develop hypotheses about their phylogenetic histories. This will allow us to determine how frequently such traits are lost and gained, the degree to which phylogenetic patterns are consistent with the hypothesis of coevolution, and whether certain evolutionary pathways are more likely than othersZ6, perhaps because of differential costs of resistance or virulence associated with different pathways. For example, do we see the independent evolution of resistance characters in many lineages, or are certain resistance traits ancestral, and thus their appearance throughout a lineage simply a reflection of historical development? Analyses of Ehrlich and Raven’s hypothesis4 of ‘escape and radiation’ coevolution have led to varied results, depending on the system studied and systematic interpretation used28. A similar emphasis on macroevolutionary trends is generally lacking in studies of plant-pathogen interactions in natural systems. Because the traits under consideration (e.g. secondary compounds) are likely to respond in evolutionary time to both herbivores and pathogens, ideally both sets of plant enemies should be considered in interpretation of patterns. An integratedapproach Clearly, approaches to the study of plant-herbivore and plantpathogen interactions often differ. These differences result from historical research trends (for example, the early emphasis on secondary chemicals and herbivores) and the practicalities of working with different organisms. Because the two sets of interactions are similiar, researchers can gain insights by borrowing approaches commonly used in the other discipline. However, we should not ignore the possibility that herbivores and pathogens may differ fundamentally in their evolutionary interactions with their plant hosts. For example, does the prevalence of asexual reproduction in many pathogenic fungi mean that coevolution could
proceed in a different way than expected with herbivorous insects? It is not a trivial task to adopt a more comprehensive view of one’s study system if it includes numerous herbivore and pathogen species. In order to study multiple species, the number of experimental treatments and field measurements required increases dramatically, and the potential for complex interactions makes data interpretation difficult. However, our understanding of the evolution of certain traits will be limited as long as we ignore the role of herbivores in plant-pathogen interactions and vice versa. Some systems, in which two interactors significantly affect the third, have already demanded an analysis of multiple herbivores and pathogens ‘**23.Results of these studies suggest that an integrative approach can be insightful, and worthy of greater attention in the future. Even if one’s research remains focused on a herbivore or pathogen, the parallels between the fields require a broader crossfertilization of ideas than currently exists. Acknowledgements We thank j. Burdon. I. Frazee, C. Hochwender, C. Israel, C. Kelly, M. Parker, N. Schellhorn, E. Simms, K. Stowe, E. Wienerand three anonymous reviewers for their comments on earlier drafts of this paper.
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