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Environmental Variation Mediates the Deleterious Effects of Coleosporium Ipomoeae on Ipomoea Purpurea

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Environmental Variation Mediates the Deleterious Effects of Coleosporium Ipomoeae on Ipomoea Purpurea Ecology, 87(3), 2006, pp. 675±685 q 2006 by the Ecological Society of America ENVIRONMENTAL VARIATION MEDIATES THE DELETERIOUS EFFECTS OF COLEOSPORIUM IPOMOEAE ON IPOMOEA PURPUREA JOEL M. KNISKERN1 AND MARK D. RAUSHER Department of Biology, Duke University, Durham, North Carolina 27708 USA Abstract. Variation in the environment is common within and between natural popu- lations and may in¯uence selection on plant resistance by altering the level of damage or the ®tness consequences of damage from plant enemies. While much is known about how environmental variation in¯uences the amount of damage a plant experiences, few studies have attempted to determine how variation in the environment may alter the ®tness con- sequences of damage, particularly in plant±pathogen interactions. In this work we manip- ulated a rust pathogen, Coleosporium ipomoeae, in ®eld experiments and showed that this pathogen reduced several components of ®tness in its natural host plant, Ipomoea purpurea. Furthermore, we showed that the deleterious effects of C. ipomoeae were variable. We identi®ed variation in the quality of a plant's microenvironment, the abundance of secondary enemy damage, and the length of a growing season as variable components of the envi- ronment that may in¯uence the magnitude of damage and tolerance, causing the interaction between C. ipomoeae and I. purpurea to vary from parasitism to commensalism. Consid- ering how environmental variation impacts the magnitude and negative ®tness effects of pathogen damage is important to understanding spatially variable selection and coevolution in this and other plant±pathogen interactions. Key words: Coleosporium ipomoeae; compensation; environmental variation; Ipomoea purpurea; phytometer; plant±pathogen interactions; tolerance. INTRODUCTION evidence suggests that variation in the biotic environ- In theory, environmental variability is likely to have ment may have similar effects. For example, damage a large effect on the evolution of plant resistance to by one pathogen can reduce the amount of damage natural enemies (pathogens and herbivores). For ex- imposed by a second pathogen by inducing systemic ample, if resistance is costly, variation in pathogen resistance (Burdon 1987, Karban and Baldwin 1997). abundance can prevent the ®xation of resistance alleles Spatial or temporal variation in the abundance of the (Gillespie 1975, Antonovics and Thrall 1994). Simi- ®rst pathogen would then presumably cause variation larly, habitat heterogeneity could potentially maintain in the magnitude of selection imposed by the second. resistance polymorphisms if the bene®ts of resistance Similarly, several investigations have demonstrated di- are greater than the costs in some habitats, while the rectly that the presence/absence of one natural enemy reverse is true in others (Levene 1953). On a larger in¯uences the magnitude, and even direction, of selec- spatial scale, geographic differences in environmental tion imposed on resistance by a second enemy (Pilson conditions may favor different levels of resistance by 1996, Juenger and Bergelson 1998, Stinchcombe and tipping the balance between costs and bene®ts in op- Rausher 2001). posite directions (Thompson's geographic mosaic the- A relatively unexplored route through which envi- ory of coevolution; Thompson 1994). ronmental variation may in¯uence the magnitude of Considerable evidence indicates that variation in abi- selection on resistance involves environmental effects otic environmental components such as temperature, on tolerance. Tolerance is distinct from resistance, in rainfall, humidity, light intensity, and nutrient gradients that resistance re¯ects the amount of damage imposed can alter the severity of herbivore or pathogen damage, by a pathogen or herbivore on a plant under constant and hence the potential for selection for resistance, by conditions, while tolerance re¯ects the impact on ®t- in¯uencing the strength of plant resistance, enemy ness of a given amount of damage (Strauss and Agrawal abundance, and enemy performance (reviewed in Bur- 1999). Environments that increase the strength of tol- don 1987, Smith 1989, Kennedy and Barbour 1992, erance will reduce the potential bene®ts of resistance Jarosz and Davelos 1995). In addition, accumulating alleles by decreasing the ®tness increase associated with being resistant. Manuscript received 26 August 2005; accepted 8 September A small number of studies show that environmental 2005. Corresponding Editor: S. H. Faeth. variation in¯uences the magnitude of tolerance to her- 1 Present address: Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637 USA. E-mail: bivory in natural populations (Maschinski and Whit- [email protected] ham 1989, Juenger and Bergelson 1997, Huhta et al. 675 676 JOEL M. KNISKERN AND MARK D. RAUSHER Ecology, Vol. 87, No. 3 2000, Levine and Paige 2004). However, we are aware I. purpurea, we employed a somewhat complicated of only one study showing how the environment may crossing design to generate seeds of all three genotypes in¯uence tolerance to disease in a natural population. at the resistance locus (see Appendix A). However, the Thrall and Jarosz (1994) reported that the difference data examined in the current report represent only the in overwintering mortality between Silene alba plants plants lacking the resistance allele, since tolerance in infected and not infected with the pathogen Ustilago this interaction is best estimated in susceptible plants. violacea decreases with the severity of winter condi- tions. Because few investigations have attempted to 2000 Field experiment determine how variation in either the abiotic or biotic A total of 864 seeds (288 each of the three genotypes environment in¯uences the magnitude of tolerance, it at the resistance locus) were planted in a randomized remains unclear how important this type of variation block design in an experimental ®eld in Durham, North may be in causing variation in the potential for selec- Carolina, on 17 July 2000. Seeds were planted at 0.75 tion on resistance. 3 1 m intervals and allowed to twine up 2-m wooden In this investigation, we examined the effect of dif- stakes. Three different treatments were imposed to ma- ferent types of environmental variation on the mag- nipulate the abundance of C. ipomoeae: (1) A patho- nitude of damage and tolerance in the common morning gen-exclusion treatment was established by spraying glory, Ipomoea purpurea, to a fungal pathogen, Co- plants with the systemic fungicide Ridomil Gold (Syn- leosporium ipomoeae. We demonstrate that spatial var- genta Crop Protection, Greensboro, North Carolina, iation in microhabitat suitability appears to modify the USA). A separate ®eld experiment in 2000 showed Ri- magnitudes of both damage and tolerance. We also ®nd domil Gold had no effect on I. purpurea size or seed that these effects are sometimes large enough to convert production in the absence of C. ipomoeae (see Appen- the interaction between C. ipomoeae and I. purpurea dix B). (2) A pathogen-addition treatment was imposed from a parasitism to a commensalism. Finally, we dem- by spraying the underside of each leaf with an aqueous onstrate that variation in damage by other natural en- solution of urediospores. This solution was made by emies, as well as variation in growing season length, rinsing the urediospores from leaves collected from may affect C. ipomoeae damage, and thereby in¯uence many plants from local populations of I. purpurea and the effect of C. ipomoeae on I. purpurea ®tness. I. hederacea. Although we do not know the number of different pathogen genotypes included in this solution, MATERIALS AND METHODS all experimental plants received the same mixture of genotypes at the same relative concentrations and den- Natural history sity. (3) Finally, a control treatment was administered Ipomoea purpurea is a self-compatible, annual plant by spraying plants with water to allow unmanipulated that is naturally infected by the fungal rust pathogen, infection by C. ipomoeae. Treatments were ®rst im- Coleosporium ipomoeae. I. purpurea ranges from Mex- posed when local populations of I. purpurea provided ico through the central, southern, and southeastern enough urediospores for the pathogen-addition treat- United States in North America. C. ipomoeae is a het- ment and were administered every two weeks there- eroecious rust fungus that is found throughout the after. Americas, and in North America is distributed from Damage by C. ipomoeae was estimated near the end Mexico east to Florida and north to Pennsylvania and of the growing season as the total percent of leaf area Illinois. Plants in the genus Pinus serve as the primary covered by uredia (fruiting bodies that produce ure- host for C. ipomoeae and may include P. palustris, P. diospores) or telia (fruiting bodies that produce telio- rigida, P. echinata, and P. taeda; the latter two species spores that do not reinfect Ipomoea). Total leaf area on are the most likely primary host species in North Car- a plant was estimated from a regression of leaf length olina (Simms 1993). Secondary hosts include several on leaf area. Damage was estimated using a clear plas- species in the genus Ipomoea (Rhoads et al. 1918). In tic grid to measure leaf area occupied by C. ipomoeae. the location of the present study (Durham County, Proportion damage was then estimated by dividing leaf North Carolina), C. ipomoeae is commonly found in area damaged by total leaf area. Plant size was esti- natural populations on I. purpurea, I. hederacea, I. coc- mated by counting the total number of leaves per plant. cinea, I. lacunosa, and I. pandurata (J. Kniskern, per- The female component of plant ®tness was estimated sonal observations). by collecting all seeds and counting the total number The data on environmental effects on damage and of seeds per plant. While no microbial pathogens other tolerance reported here are derived from three similar than C. ipomoeae were visible in 2000, we estimated ®eld experiments performed in successive years. Pop- the percent leaf area removed by insect herbivores as ulations of I. purpurea are typically polymorphic at a described previously.
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