Lack of a tradeoff between constitutive and induced defenses among varieties of cotton

Transcription

1 OKOS 65: 3-36, Copenhagen 992 Lack of a tradeoff between constitutive and induced defenses among varieties of cotton Alison K. Brodv and Richard Karban Brody, A. K. and Karban, R Lack of a tradeoff between constitutive and induced defenses among varieties of cotton. - Qikos 65: Selecting crop plants for high yields has been associated with reduced levels of resistance against herbivores. This raises the concern that varieties selected for high levels of constitutive resistance may have reduced levels of induced defenses. nduced resistance has been hypothesized to evolve in plants when constitutive defenses are costly and not always beneficial. n this study we examined the relationship between constitutive resistance against spider mites and induced resistance against mites and verticillium wilt in ten varieties of cultivated cotton known to possess different levels of constitutive resistance. Levels of constitutive resistance against spider mites were estimated as the number of mites that were found on undamaged plants. Levels of induced resistance against mites were estimated by calculating the percent reduction in mite populations on plants that had been previously damaged relative to undamaged controls. nduced resistance against verticillium wilt was assayed by comparing the number of mitedamaged plants that recovered from exposure to the disease versus the number of undamaged control plants that recovered. We found no evidence for a negative eorrelation between levels of constitutive and induced resistance against mites. Similarly, we found no evidence of tradeoffs between constitutive resistance to mites and induced resistance against verticillium wilt. Selecting plants for high levels of constitutive defenses should not necessarily bring along with it the unwanted consequence of lowered levels of induced resistance..4. K. Brody and R. Karban. Dept of Entomotogy. Univ. of Catifornia. Davis. CA 9566, US A (present address of A KB: Rocky Mountain Biotogicat Laboratory, Crested Butte. CO USA). t is a widely held belief that breeding crop plants for increased yields has caused a decrease in the levels of resistance of those lines against insects (Feeny 976, Janzen 973, Kogan 986, Pimentel 986). The most frequently cited explanation for such a negative association relies on the assumption that botb high yields and defense require costly energy or nutrients; plants that allocate more to one function will have less to allocate to other functions. Substantial evidence exists for negative phenotypic tradeoffs between yields and resistance (Pimentel 977, Krischik and Denno 983), although the underlying genetic constraints are rarely known (Gould 983). n the case of cotton, for example, breed- ing efforts during the late 94s, 95s, and early 96s selected for varieties that were the highest yielding and were reproductive over much of the season; these varieties were generally highly vulnerable to insect attack (Bottrell and Adkisson 977). f there arc indeed tradeoffs between plant allocation to reproduction and to resistance incurred when breeding for high yields then the same constraints may cause tradeoffs between different modes of resistance (constitutive vs induced) or between resistance against different types of plant parasites (chewing insects, sap feeding insects, fungal diseases, etc). For example, pubescent varieties of cotton were found to be more resistant to Accepted 23 January 992 OKOS OKOS 65:2 (992) 3

2 jassids but more susceptible to several Lepidoptera (Batra and Gupta 97). A theory based on the notion that defenses are costly has led to speculation that induced resistance may allow plants to save valuable resources. nduced resistance, by definition, is activated only after a plant receives damage, or cues of pending damage, from its parasites (Karban and Myers 989), We use the term resistance to indicate that a plant trait negatively affects herbivore preference or performance. n contrast, a defense increases plant fitness and likely (though not necessarily) evolved in the context of providing resistance. t has been speculated that resistance is costly to plants in terms of rcst)urccs that could be used in other ways to increase plant fitness (Haukioja and Niemela 979, Rhoades 979). Plants with preformed defenses will have "wasted resources" when those defenses do not protect them from fitness reductions caused by herbivory. Such wastage can come about if defenses are not effective or if the plants are not attacked by herbivores. As a result, induced resistance is expected to evolve in plants when defenses are costly and not always required (Haukioja and Niemela 979, Mattson et al. 988, Karban and Myers 989). Plants with high levels of constitutive resistance against a particular parasite are not expected to also possess induced resistance against that attacker. n this we assume ) that the resource budget of a plant is fixed, 2) that constitutive and induced resistance have evolved as defenses and may act independently of one another, and 3) that both types of resistance exact a significant cost to plants' resources. The study we report here examines whether tradeoffs exist between levels of constitutive and induced resistance among varieties of cultivated cotton. Damage to cotton cotyledons (Gossypium hirsutum, var. Acala SJ-2) increased resistance in the growing seedling as assayed by the population growth of mites (Tetranychus urticae) (Karban and Carey 984). For spider mites, reduced population growth caused by induced resistance acted primarily via lower fecundity and not by large differences in survival (Brody and Karban 989). nduced resistance in cotton is a generalized response to wounding and has activity against a variety of mites, insects, and pathogens (Karban et al. 987, Karban 988), For example, seedlings (variety Acala SJ-2) that were damaged by spider mites became more resistant against the symptoms of verticillium wilt (Karban et al. 987). Different varieties of cultivated cotton have been found to have different levels of constitutive resistance to spider mites {T. urticae) (Schuster et al. 972). We selected varieties with known differences in constitutive resistance and examined patterns of variability in their levels of induced resistance against spider mites and verticillium wilt. 32 Methods Cotton seeds of ten varieties (Coker looa, Deltapine 6, Deltapine Smooth, Dixie King, M8, Mil, Pima S4, Stardel, Stoneville 7A, and Wescot) were obtained from Dr. A, E. Percival, USDA Crop Germplasm Research Unit, College Station, Texas. These ten varieties are not a random sample of the gene pool of wild Gossypium hirsutum, they were all selected as high yielding cultivars. However, they were chosen for this study because they spanned the reported range of constitutive resistance against spider mites (Schuster et al. 972). For experiments involving spider mites only, seeds were sown into four inch pots ( seed per pot) and grown at 28 C, L:D 4; in a Sherer/Rheem chamber. Four plants (pots) of each variety were used in each experiment; two pots were assigned to be damaged and two were undamaged controls. When plants had expanded their cotyledons but before they had any true leaves, those scheduled for damage were infested with adult female spider mites {Tetranychus turkestani). Each plant (of both treatments) was enclosed in a sleeve of acetate to prevent movement of mites between plants. Mites were allowed to feed for five d, at which time mite-infested and control plants were dipped in miticide (dicofol, ppm) which killed all mites. The plants were then allowed to grow, free of mites for 4 d, at which time they typically had two or three true leaves. Three adult female mites {Tetranychus urticae) were placed on the most recently expanded leaf of each plant. The mites were allowed to feed and reproduce for 4 d (approximately.5 generations) at which time all mites and eggs were counted. The experiment was repeated four times from autumn 988 to spring 989 using the same growth chamber. Two experiments were also performed to test for resistance against Verticilliutn dahliae induced by damage caused by spider mites. These experiments were begun in November 989 and February 99 and included 4 and 3 replicates (plants), respectively, of each treatment for each of the ten varieties. n these two experiments which were conducted in a greenhouse in Davis, the procedure was the same as that described above, up to and including the time when mites were removed by treating all plants with miticide. When the plants were typically at the 3-leaf stage they were each challenged by inoculation with a suspension of Verticilliutn conidia (strain SS-4,. optical density or approximately 7 viable conidia per ml). Three injections were made into the upper stem of each plant (see Schnathorst and Mathre 966 for detailed methods). Plants were checked weekly over the next 8 weeks. Regression analysis (GLM procedure, Systat, Evanston, L) was used to examine the relationship between levels of constitutive resistance against mites and levels of induced resistance against both mites and verticillium wilt. We used the mean number of mites counted on our undamaged control plants as an estimate of constitutive OKOS 65:2 (992)

3 ihgh Expt, u> c ' o E o 8 D HGH Z o Expt " m Number of Mttes on Control Plants HGH Number of Mites on Control Plants HGH Fig.. The correlation between constitutive and induced resistance against spider mites for varieties of cotton in four experiments. Constitutive resistance was estimated by the number of mites found on undamaged control plants. High mite numbers indicate low resistance. ndueed resistance was estimated by the percentage reduction in mite numbers on induced plants relative to controls. Plants with high induced resistance have relatively fewer mites on damaged plants compared to undamaged controls. resistance against mites for each variety. Varieties with fewer mites had higher levels of constitutive resistance. The strength of induced resistance against mites was estimated as the percent reduction in mite numbers on damaged plants relative to controls ([number of mites on controls - number of mites on damaged plants] / number of mites on controls). Whenever fractions were used in analyses, they were transformed using an angular transformation although information presented in figures was not transformed. Varieties with high levels of induced resistance had proportionally fewer mites on damaged plants compared to controls. As a measure of induced resistance against verticillium wilt, we used the number of mite-damaged plants that recovered (as opposed to died) from the fungal disease minus the number of undamaged control plants that recovered. For varieties with high levels of induced resistance more plants recovered from the fungal disease that had been damaged by mites than had not been damaged. Our estimate of resistance against mites is based on the growth of the mite population while our estimate of resistance against the fungus is based on plant survival. Although these two are not directly comparable, high numbers of mites reduce plant survival (Wilson 99) and plant reproduction (Canerday and Arant 964, Leigh et al. 968, Mistric 969). Results The population growth of spider mites varied by an order of magnitude among the experiments (Fig. ; plants in experiment 2 conducted during winter had a mean of 6.3 ± 3.3 mites while those in experiment 3 OKOS 65:2 (W2) conducted during spring had 93 ± 8.9 mites). This very large seasonal variation is discussed in detail elsewhere (Karban 987). Levels of constitutive resistance were not associated with levels of induced resistance in any of the four experiments (Fig. ). ndeed, in experiments and 3 the direction of the association between the two forms of resistance was negative while in experiments 2 and 4 the direction was positive (Expt : regression coefficient =.94, F,, = 4., P = O.(J8; Expt 2: regression coefficient = -.23, F, 7 =.6, P =.82; Expt 3; regression coefficient = -.2, F, 7 =.3, P =.86. One plant of varieties Stardel and Stoneville 7A died in expts 2 and 4, respectively). When all four experiments were considered together, there was similarly no indication of a tradeoff between constitutive and induced resistance against mites (Fig. 2, R =.57, Regression SS = 86.93, Error MS = 43.27, F,, =.2, P =.67). Tbe power of this test was.3 (Zar 984: 34); in other words we cannot conclude that a tradeoff does not exist but only tbat we failed to find one. Our ability to detect a significant relationship (alpha =.5) was low because we only had independent points. A previous study also independently measured levels of constitutive resistance of these varieties against spider mites (Schuster et al. 972). A significant relationship was found between our estimates of constitutive resistance and their measures of tbe number of eggs produced by females of T. urticae during 72 h (F, ^ - HGH DU» Pima!34 Dellapine Smooth Q. o 5 M 4 - OC Coker A 3 - Stoneville 7A 2 Wescot c o Deltapine 6 Stardel a> OC Dixie King - V M Number of Mites on Control Plants HGH Fig. 2. The correlation between constituti\e and mduced resistance against spider mites. Each point is the mean \ alue for one variety in four experiments. Constitutive resistance was estimated by the number of mites found on undamaged control plants. High mite numbers mdicate low resistance ndueed resistance was estimated by the percentage reduction in mite numbers on indueed plants relative to controls. Plants with high induced resistance have relatively fewer mites on damaged plants compared to undamaged controls. 33

4 HGH o Discussion ) S 2. CC o.5 ( CE.c - ( ro «Coker A M..5 ^'X"^^^ Sioneville 7A - * i Pima S-4 Dellapine 6 M a> ^ = o Deltapine Smooth Dixie King -. Wescot Number of Mites on Control Plants HGH «Fig. 3. The correlation between constitutive resistance against spider mites and induced resistance against Verticittium dahtiae for varieties of cultivated cotton. Constitutive resistance was estimated by the number of mites found on undamaged control plants. nduced resistance against verticillium was estimated as the difference in number of plants that recovered from the disease that had been first damaged by mites minus undamaged control plants that recovered. 5.38, P =.49). f their independent measure of constitutive resistance was used in the analysis, there was no evidence of a tradeoff with induced resistance against mites (F,,, =.449, P =.522). Results were similar if other measures of constitutive resistance (i.e. /fecundity, fecundity x survival, damage to the plant) or of induced resistance (i.e. [mean number of mites on controls - mean number of mites on damaged plants]) were used in the analysis. Varieties that had high levels of constitutive resistance against mites were no less likely to have high levels of induced resistance against verticillium wilt (increase in the likelihood that mite-damaged plants would recover from the fungal disease). To the contrary, varieties with high levels of constitutive resistance against mites also tended to have high levels of induced resistance against Verticillium fungi although this trend was not statistically significant (Fig. 3; F.^ = 2.94, P =.26). However, if Schuster's independent estimate of constitutive resistance (Schuster ct al. 972) was used in the analysis, constitutive resistance against mites and induced resistance against verticillium were positively associated (F,, = 5.375, P =.49). We found no significant relationship between induced resistance against mites and induced resistance against verticillium wilt in these cultivars (F,, =.332, P =.58). 34 The lack of a tradeoff (negative correlation) between levels of constitutive resistance and levels of induced resistance against mites (Figs and 2) was contrary to our initial expectations. nterpretation of these negative results must be tempered because our experiment had relatively weak power to detect such effects. Nonetheless, many of the varieties with high constitutive resistance also were amongst the ones for which induced resistance against mites was the strongest (Pima S-4, M, Coker looa, Stoneville 7A). Those varieties with the biochemical mechanisms for constitutive resistance against mites may also be the ones that can activate such a mechanism in response to attack. ndeed, most ofthe compounds which are known to provide resistance in cotton against mites and other agents can also be induced by damage (Bell 986). The results involving verticillium wilt (Fig. 3) lend even less support for the notion that constitutive and induced resistance will be negatively correlated. The relationship we found was one of a positive association rather than a tradeoff. Our results were similar to those found by several other researchers. n a comparison of resistance of two soybean cultivars to spider mites, the variety with more constitutive resistance also showed a stronger hypersensitive response to mite damage (Hildebrand et al. 986). Similarly, the more resistant of two strawberry cultivars showed a greater induced response to mite damage, measured in terms of mite-feeding preference (Kielkiewicz 988). n a study of lupines, Johnson et al. (989) found that leaves with the highest initial levels of alkaloids were the ones with the greatest induced increases relative to undamaged controls. Cultivated varieties of cotton may not be the best model system to find tradeoffs between constitutive and induced resistance. Tbe plants probably did not evolve in an environment in which spider mites or verticillium wilt exerted much selective force. However, the induced response in cotton seedlings is a generalized response caused by many different insects and diseases and also effective against a wide variety of organisms (Karban et al. 987, Karban 988). As a group, parasites such as these must have exerted selective pressure. A tradeoff was expected between constitutive and induced resistance because defenses were assumed to be costly and induced resistance was assumed to be one means of reducing the "cost of defense \ Although the notion that plants should not invest in costly and redundant systems of defense is widespread, we know of only two other studies that explicitly looked for tradeoffs between such systems. Steward and Keeler (988) examined the presumed defenses found in 9 species of pomoea and failed to find evidence for tradeoffs; there was no tendency for species having one defense to lack others. Zangerl and Berenbaum (99) found positive, rather than negative, genetic correlations between levels of constitutive and induced furanocoumarins in wild OKOS 65:2 (992)

5 parsnip individuals. However, plants from a population which incurred more herbivore damage had higher levels of constitutive furanocoumarins to begin with compared with a population which was less often subjected to attack. Because cultivated cottons have been subjected to selection for increased yields and now face different herbivores and diseases than the ones that they evolved with, it is not clear how much we can learn about the evolution of defenses from this system. Furthermore, we measured the outcome of cither constitutive or induced resistance and make inferences about the investment in these two forms. f the outcome of resistance does not reflect the plant s investment then we would not necessarily expect a trade-off between the two forms of resistance. Our failure to find any evidence of tradeoffs between constitutive and induced defenses in these cottons is evidence that the two are probably not negatively correlated. f effectiveness, rather than cost, provides the primary advantage of a defense that changes rapidly then there is no reason to expect a tradeoff between constitutive and induced defenses. Selecting plants for high levels of constitutive defenses should not necessarily bring along with it the unwanted consequence of lowered levels of induced resistance. Acknowtedgements - A. E. Percival graciously pri>vided the seeds used in the experiments. A. Donatelli. G. English-Loeb, and W. Schnathorst assisted with lab work and H. Dingle. E. Haukioja, S. Strauss, N. Willits, and T. Young improved the manuscript. This work was supported by USDA grants S-25 and to R.K. References Batra, G. R. and Gupta. D. S. 97. Screening of varieties of cotton for resistance to jassid. - Cotton Growing Review 47: Bell. A. 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Academic Press, New York, pp Haukioja, E. and Niemela, P Birch leaves as a resource for herbivores: Seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. Oecologia 39: OKOS 65:2 (W2) Hildebrand. D. F, Rodriguez. J G.. Brown, G. C. and Volden, C. S Twospotted spider mite (Acari: Tetranychidae) infestations on soybeans: effect on composition and growth of susceptible and resistant cultivars. - J. Econ. Entomol. 79: Janzen, D. H Tropical agroecosystems. - Science 82: Johnson, N. D., Rigney, L. P. and Bentley. B. L The short-term induction of alkaloid prtiduction in lupines: differences between N2-fixing and nitrogen-limited plants. - J. Chem. Ecol. 5: Karban, R Environmental conditions affecting the strength of induced resistance against mites in cotton. Oecologia 73: Resistance to beet armyworms {Spodoptera exigua) induced by exposure to spider mites (Tetranychus turkestani) in cotton. - Am. Midi. Nat. 9: and Carey, J. R nduced resistance of cotton seedlings to mites. - Science 225: and Myers, J. H nduced plant responses to herbivory. - Annu. Rev. Ecol. Syst. 2U: , Adamchak. R. and Schnathorst, W. C nduced resistance and interspecific competition between spider mites and a vascular wilt fungus. - Science 235: 67S-68. Kielkiewicz. M Susceptibility of previously damaged strawberry plants to mite attack. - Entomtil. E.xp. Appl. 47: ' Kogan, M Plant defense strategies and host-plant resistance. - n: Kogan. M. ( e d ). Ecological theory and integrated pest management practice. Wiley-nterscience, New York. pp Krischik. V. A. and Denno, R. F ndividual, population, and geographic patterns in plant defense. - n: Denno, R. F. and McClure, M. S. (eds). Variable plants and herbi\ores in natural and managed Systems. Academic Press, New York. pp Leigh, T. F. Hunter, R. E. and Hyer. A. H Spider mite effeets on yield and quality of four cotton varieties. - California Agriculture 22: - 5. Mattson, W. J.. 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6 spider mite on cotton in Australia and implications for induction in wild parsnip: genetics and populational varmanagement. - Ph.D. thesis, Dept of Entomology, Univ. iation. - Ecology 7: of Queensland. Zar, J. H Biostatistical analysis. 2nd ed. - Prentice-Hall, Zangerl, A. R. and Berenbaum, M. R. 99. Furanocoumarin Englewood Cliffs, NJ. 36 OKOS 65:2

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