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Fungal pathogens affect plant population dynamics and evolution
attack mainly when light levels were relatively high. In natural Trinidadian streams this tendency was more obvious, with most predation occurring towards midday. This was true for Astyanax bimaculatus and Hemibrycon dentatum, two other guppy predators, as well. But is the relationship between peak predation risk and peak conspicuousness causal? During equivalent periods before and after C. alta was introduced into the artificial stream there was a significant difference in guppy behaviour. With the predator present, the conspicuous elements of courtship behaviour, such as displays and chases, diminished, while other less conspicuous elements, such as sneaky copulation attempts, increased. Intense light inhibits conspicuous male courtship behaviour in guppies because, argues Endler, it is a reliable cue for high predation risk in the wild where predators generally hunt around
midday. The response occurs even when predators are not present. But adding a predator enhances the response, as expected. So, selection has armed guppies with a behavioural solution for avoiding the compromise between conspicuousness and crypsis. But the need to remain relatively cryptic at midday doesn’t stop males mating altogether. Instead there is a switch towards the much less conspicuous sneaky copulation strategy. But, if sneaky copulations are safer, why don’t males use this strategy all the time? The answer is that it is not as successful. When females are at the correct stage of the ovarian cycle they become receptive and undergo long bouts of standard copulation with a displaying male, and stored sperm from previous males is displaced. Sperm from a sneaky mating will rarely achieve fertilization because a standard mating will usually follow when the female is finally re-
Fungal Pathogens AffectPlantPopulation Dynam and ics Evolution PauletteBierzychudek As A PLANT POPULATION BIOLOGIST, I have always viewed fungal pathogens as a messy complication. I tend to exclude infected individuals from population samples, since, after all, such individuals can hardly be expected to behave normally. I suspect that my attitude is not uncommon. However, the work of a few innovative population biologists is now plant’s that a reminding us pathogens can be just as important a selective force as its pollinators, competitors and herbivores, and just as worthy of study. Until just a few years ago, most of what we knew about the interactions of plants and their pathogens came from crop plants, or from studies conducted in controlled environments. The recent studies reported below are notable exceptions, and attempt to answer at least one of the following questions: (1) what effect, if any, do fungal pathogens have on the fitness and/or population dynamics of their hosts? (2) do host Paulette Bierzychudekis at the Dept of Biology, Pomona College, Claremont, CA 91711, USA,
and the Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA.
6
individuals or species vary in their susceptibility to infection, or in their suitability as hosts? (3) what effects are such pathogens likely to have on the evolution of disease resistance in host populations? Evidence is accumulating that fungal pathogens can have dramatic negative effects on the fitness of individuals, with important impacts on the population dynamics and evolution of their hosts. Interestingly, though pathogens are typically assumed to act in a densitydependent manner, most studies have not found disease incidence to be correlated with plant density’,’ (but see Ref. 3). One of the most interesting studies of pathogen impact has been carried out by Parker2, working in Illinois on jack-in-the-pulpits, Arisaema triphyl/urn, a forest understory herb that is attacked by the fungus Uromyces ari-triphylli. The incidence of infection at Parker’s sites ranged from 7% to 42%. He found that infected individuals produced 42% fewer cormlets (asexual progeny) than healthy plants, and that the cormlets of diseased individuals invariably were themselves diseased. Although the seed production of diseased plants
ceptive. As long as he IS relatively safe from predators it still pays a male guppy to show off his vigorous courtship display. References 1 Darwin, C. (18711 Tt7eDescentofMan, and Selectmn in Reiatmn to Sex, John Murray 2 Guilford, T.C. and Dawkins, M.S (1987! An/m. Behav. 35,1838-1845 3 Endler, J.A. (1978) Evol. Bioi. 1 1, 319-364 4 Endler, J.A (19841 Bioi .i. iin~. SOL 27, 187-231 5 Endler. J.A. 11Y86) in i’redator- Pq Relationships: Perspectives and Approaches fro/n the Study of Lower Vertebrates (Feder, M.E. and Lauder. G.V., eds), pp. 109-134, University of Chicago Press 6 Endler, J.A. (1987) A~jn?. Behab” 35 1376-1385 7 Endler, J.A. i 1980) E ’vo/~1t~u7 34, 76.-9 i 8 Endler. J.A. 11982) Evolution 36.
was reduced by 79%, seeds of infected individuals were never observed to carry the disease. Thus, seed production provides the only means by which progeny can escape from their parent’s pathogens, and Parker suggests that fungal infectiorl may serve as an important selective agent maintaining sexual reproduc tion in A. triphyllum. While this phenomenon has often been sug gested as an irnportant advantage of sexual Parker’s reproduction4-6, work is among the first supportive field evidence. Not all studies have dernonstrateu purely negative effects on plant fit ness. Clay, working on the grass Danthonia spicata and its endophytic fungus, Atkinsonella hypoxylon. suggests that other kinds of interactions
are
infected ducing
also
possible’,
hosts were obligately
limited
self-fertilized
Although
to proseed,
they were significantly larger and produced more inflorescences than uninfected Individuals did when competing with the grass Anthoxan thum odoratum’. Clay suggests for this greater
possibility resistance
as one mechantsm vegetative vigor the
that the fungus confers to herbivory. Atkinsonella
and other members of the Balansiae (like their close relative Claviceps, the ergot fungus) produce toxic alkaloids. Greenhouse experiments by Clay and Cheplick” with a variety of grass species and fall armyworms ir’r generalist herblvorei showed slgnificant decreases in larval survival and pupal weight for armyworm indi
TREE vol. 3, no. 1, January
1988
vijuals reared on tissue from infezted grasses. Clay and Cheplick interpreted these results as evidence that fungal alkaloids deter the insect herbivores of these grasses, and that therefore the grass-fungus interaction is a mutualistic one. However, they have not yet measured the fitnl?ss of infected and uninfected plants under field conditions. In order for fungal pathogens to act as selective agents shaping the genetic characteristics of plant populations, there must be genetic variability among host individuals in their susceptibility to fungal infection. Alexander” has found signific;lnt inter-clone variation in susceptibility to infection of Silene alba to Ustilago violacea, with some genotypes never becoming infected, and others always succumbing. Additional work on variation has been carried out by Parker working OII Amphicarpaea bracteata, an annual legume infected by Synchytn~rn decipiens. Parker’s work”-‘5 is tt e most elegant and insightful of all o’ these studies, and has the most far-reaching evolutionary implicativlns. By infecting plants from sevelal populations with fungal spores from their own and from other pf,pulations, Parker obtained the somewhat surprising result that A. b-acteata families showed the least nmsistance to S. decipiens strains from their own populations”. He ai.gued that these results implied the e.tistence of constraints on the e’/olution of disease resistance, and set out to explore their nature. Parker focused on three classes of (ilot mutually exclusive) constraints: (“) populations might lack genetic v.3riability for disease resistance; (2) resistance might entail costs that balaice its benefits; and (3) a plant’s mating system might constrain the \hay genetic variation is organized aid made available for selection. Parker’s work suggests that at least two of these constraints are in fact ooerating. He screened A. bracteata families for resistance to three pathogen strains, and found no resistance at all to two of the isolates, aid resistance to the third in only 11% of families l3 . Although alleles c,lnferring resistance do exist in rearby populations, the limited seed dispersal in this species apparently limits the rate at which they might Plove between populations. Thus, I;ilck of genetic variability does aapear to be an important evolutiona ry constraint. What about the idea of tradeoffs between the costs and benefits of resistance? Because resistance is conferred by a dominant allele at a
single Iocu~‘~, Parker was able to create a hybrid family, which produced two lineages homozygous for resistance, and two others homozygous for susceptibility. When in the absence of the grown pathogen, these individuals provided no evidence that bearing the resistance allele decreased an individual’s fitness in any way”. Finally, Parker carried out an electrophoretic analysis of A. bracteata seeds and found evidence of strong inbreeding and gametic disequilibrium14. Though A. bracteata produces both chasmogamous (outcrossed) and cleistogamous (obligately self-fertilized) flowers, only a small minority of seeds came from the chasmogamous flowers’5. Despite Hardy-Weinberg expectations of 40% heterozygotes, heterozygote frequency was in fact less than l%, with the population dominated by just a few multilocus genotypes14. ‘Susceptible’ and ‘resistant’ biotypes had different alleles at multiple allozyme loci, and also differed in several other phenotypic traits, such as leaf morphology, flower color, and seed weight. Selection for any of these traits could potentially interfere with the evolution of resistance, and Parker is currently measuring selection on these phenotypic characters. illustrate studies that These pathogens possess considerable potential for influencing plant evolution. Might they also be able to direct that evolution to their own ends? Some male genotypes of Silene alba produce more flowers when they are diseased than when they are healthy”. Since fungal
spores are produced in their anthers carried by pollinators, a and pathogen that could increase its host’s flower production would increase its rate of spread. In Danthonia spicata, infected individuals abort their chasmogamous flowers, but continue to produce cleistogamous ones, which are less likely to produce new, and possibly resistant, progeny genotypes’. And in Amphicarpaea bracteata, heavily infected plants have lax, elongated stems; these plants lie close to the ground, in a moist microenvironment ideal for reinfection15. Whether these effects are fortuitous or are actually being selected for by the fungus should be an interesting question for future research.
References 1 Lee, J.A. (1981) NewPhytol. 87,81-89 2 Parker, M.A. Am. J. Bat. (in press) 3 Augspurger, C.K. and Kelly, C.K. (1984) Oeco/ogia61,211-217 4 Bremermann, H.J. (1980) ./. Theor. Biol. 87,671-702 5 Hamilton, W.D. (1980) Oikos 35’. 282-290 6 Rice, W.R. (1983)Am. Nat. 121,187-203 7 Clay, K. (1984) NewPhytol. 98, 165-175 8 Kelley, S.E. and Clay, K. (1987) Evo/urion 41,92-l 03 9 Cheplick, G.P. and Clay, K. (1987)Am. J. Bat. 74,632 (abstract) 10 Alexander, H.M. (1987)Am. J. Bat. 74, 632 (abstract) 11 Parker, M.A. (1985) Evolution 39, 713-723 12 Parker, M.A. Heredity (in press) 13 Parker, M.A. (1987) Am. J. Bat. 74,633 (abstract) 14 Parker, M.A. Evolution (in press) 15 Parker, M.A. (1986) Oecologia 69, 253-259
In the next issue of TREE * The relationships of the major groups of mammals: new approaches, M . J. Benton * Are the pyramids deified dungpats? 1,Hanski * Tamarin and marmoset mating systems, A. Goldben * The adaptive significance of play, T. M . Care * Predation may link the cycles of lemmings and arctic birds, W . J. Sutherland 7
midday. The response occurs even when predators are not present. But adding a predator enhances the response, as expected. So, selection has armed guppies with a behavioural solution for avoiding the compromise between conspicuousness and crypsis. But the need to remain relatively cryptic at midday doesn’t stop males mating altogether. Instead there is a switch towards the much less conspicuous sneaky copulation strategy. But, if sneaky copulations are safer, why don’t males use this strategy all the time? The answer is that it is not as successful. When females are at the correct stage of the ovarian cycle they become receptive and undergo long bouts of standard copulation with a displaying male, and stored sperm from previous males is displaced. Sperm from a sneaky mating will rarely achieve fertilization because a standard mating will usually follow when the female is finally re-
Fungal Pathogens AffectPlantPopulation Dynam and ics Evolution PauletteBierzychudek As A PLANT POPULATION BIOLOGIST, I have always viewed fungal pathogens as a messy complication. I tend to exclude infected individuals from population samples, since, after all, such individuals can hardly be expected to behave normally. I suspect that my attitude is not uncommon. However, the work of a few innovative population biologists is now plant’s that a reminding us pathogens can be just as important a selective force as its pollinators, competitors and herbivores, and just as worthy of study. Until just a few years ago, most of what we knew about the interactions of plants and their pathogens came from crop plants, or from studies conducted in controlled environments. The recent studies reported below are notable exceptions, and attempt to answer at least one of the following questions: (1) what effect, if any, do fungal pathogens have on the fitness and/or population dynamics of their hosts? (2) do host Paulette Bierzychudekis at the Dept of Biology, Pomona College, Claremont, CA 91711, USA,
and the Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA.
6
individuals or species vary in their susceptibility to infection, or in their suitability as hosts? (3) what effects are such pathogens likely to have on the evolution of disease resistance in host populations? Evidence is accumulating that fungal pathogens can have dramatic negative effects on the fitness of individuals, with important impacts on the population dynamics and evolution of their hosts. Interestingly, though pathogens are typically assumed to act in a densitydependent manner, most studies have not found disease incidence to be correlated with plant density’,’ (but see Ref. 3). One of the most interesting studies of pathogen impact has been carried out by Parker2, working in Illinois on jack-in-the-pulpits, Arisaema triphyl/urn, a forest understory herb that is attacked by the fungus Uromyces ari-triphylli. The incidence of infection at Parker’s sites ranged from 7% to 42%. He found that infected individuals produced 42% fewer cormlets (asexual progeny) than healthy plants, and that the cormlets of diseased individuals invariably were themselves diseased. Although the seed production of diseased plants
ceptive. As long as he IS relatively safe from predators it still pays a male guppy to show off his vigorous courtship display. References 1 Darwin, C. (18711 Tt7eDescentofMan, and Selectmn in Reiatmn to Sex, John Murray 2 Guilford, T.C. and Dawkins, M.S (1987! An/m. Behav. 35,1838-1845 3 Endler, J.A. (1978) Evol. Bioi. 1 1, 319-364 4 Endler, J.A (19841 Bioi .i. iin~. SOL 27, 187-231 5 Endler. J.A. 11Y86) in i’redator- Pq Relationships: Perspectives and Approaches fro/n the Study of Lower Vertebrates (Feder, M.E. and Lauder. G.V., eds), pp. 109-134, University of Chicago Press 6 Endler, J.A. (1987) A~jn?. Behab” 35 1376-1385 7 Endler, J.A. i 1980) E ’vo/~1t~u7 34, 76.-9 i 8 Endler. J.A. 11982) Evolution 36.
was reduced by 79%, seeds of infected individuals were never observed to carry the disease. Thus, seed production provides the only means by which progeny can escape from their parent’s pathogens, and Parker suggests that fungal infectiorl may serve as an important selective agent maintaining sexual reproduc tion in A. triphyllum. While this phenomenon has often been sug gested as an irnportant advantage of sexual Parker’s reproduction4-6, work is among the first supportive field evidence. Not all studies have dernonstrateu purely negative effects on plant fit ness. Clay, working on the grass Danthonia spicata and its endophytic fungus, Atkinsonella hypoxylon. suggests that other kinds of interactions
are
infected ducing
also
possible’,
hosts were obligately
limited
self-fertilized
Although
to proseed,
they were significantly larger and produced more inflorescences than uninfected Individuals did when competing with the grass Anthoxan thum odoratum’. Clay suggests for this greater
possibility resistance
as one mechantsm vegetative vigor the
that the fungus confers to herbivory. Atkinsonella
and other members of the Balansiae (like their close relative Claviceps, the ergot fungus) produce toxic alkaloids. Greenhouse experiments by Clay and Cheplick” with a variety of grass species and fall armyworms ir’r generalist herblvorei showed slgnificant decreases in larval survival and pupal weight for armyworm indi
TREE vol. 3, no. 1, January
1988
vijuals reared on tissue from infezted grasses. Clay and Cheplick interpreted these results as evidence that fungal alkaloids deter the insect herbivores of these grasses, and that therefore the grass-fungus interaction is a mutualistic one. However, they have not yet measured the fitnl?ss of infected and uninfected plants under field conditions. In order for fungal pathogens to act as selective agents shaping the genetic characteristics of plant populations, there must be genetic variability among host individuals in their susceptibility to fungal infection. Alexander” has found signific;lnt inter-clone variation in susceptibility to infection of Silene alba to Ustilago violacea, with some genotypes never becoming infected, and others always succumbing. Additional work on variation has been carried out by Parker working OII Amphicarpaea bracteata, an annual legume infected by Synchytn~rn decipiens. Parker’s work”-‘5 is tt e most elegant and insightful of all o’ these studies, and has the most far-reaching evolutionary implicativlns. By infecting plants from sevelal populations with fungal spores from their own and from other pf,pulations, Parker obtained the somewhat surprising result that A. b-acteata families showed the least nmsistance to S. decipiens strains from their own populations”. He ai.gued that these results implied the e.tistence of constraints on the e’/olution of disease resistance, and set out to explore their nature. Parker focused on three classes of (ilot mutually exclusive) constraints: (“) populations might lack genetic v.3riability for disease resistance; (2) resistance might entail costs that balaice its benefits; and (3) a plant’s mating system might constrain the \hay genetic variation is organized aid made available for selection. Parker’s work suggests that at least two of these constraints are in fact ooerating. He screened A. bracteata families for resistance to three pathogen strains, and found no resistance at all to two of the isolates, aid resistance to the third in only 11% of families l3 . Although alleles c,lnferring resistance do exist in rearby populations, the limited seed dispersal in this species apparently limits the rate at which they might Plove between populations. Thus, I;ilck of genetic variability does aapear to be an important evolutiona ry constraint. What about the idea of tradeoffs between the costs and benefits of resistance? Because resistance is conferred by a dominant allele at a
single Iocu~‘~, Parker was able to create a hybrid family, which produced two lineages homozygous for resistance, and two others homozygous for susceptibility. When in the absence of the grown pathogen, these individuals provided no evidence that bearing the resistance allele decreased an individual’s fitness in any way”. Finally, Parker carried out an electrophoretic analysis of A. bracteata seeds and found evidence of strong inbreeding and gametic disequilibrium14. Though A. bracteata produces both chasmogamous (outcrossed) and cleistogamous (obligately self-fertilized) flowers, only a small minority of seeds came from the chasmogamous flowers’5. Despite Hardy-Weinberg expectations of 40% heterozygotes, heterozygote frequency was in fact less than l%, with the population dominated by just a few multilocus genotypes14. ‘Susceptible’ and ‘resistant’ biotypes had different alleles at multiple allozyme loci, and also differed in several other phenotypic traits, such as leaf morphology, flower color, and seed weight. Selection for any of these traits could potentially interfere with the evolution of resistance, and Parker is currently measuring selection on these phenotypic characters. illustrate studies that These pathogens possess considerable potential for influencing plant evolution. Might they also be able to direct that evolution to their own ends? Some male genotypes of Silene alba produce more flowers when they are diseased than when they are healthy”. Since fungal
spores are produced in their anthers carried by pollinators, a and pathogen that could increase its host’s flower production would increase its rate of spread. In Danthonia spicata, infected individuals abort their chasmogamous flowers, but continue to produce cleistogamous ones, which are less likely to produce new, and possibly resistant, progeny genotypes’. And in Amphicarpaea bracteata, heavily infected plants have lax, elongated stems; these plants lie close to the ground, in a moist microenvironment ideal for reinfection15. Whether these effects are fortuitous or are actually being selected for by the fungus should be an interesting question for future research.
References 1 Lee, J.A. (1981) NewPhytol. 87,81-89 2 Parker, M.A. Am. J. Bat. (in press) 3 Augspurger, C.K. and Kelly, C.K. (1984) Oeco/ogia61,211-217 4 Bremermann, H.J. (1980) ./. Theor. Biol. 87,671-702 5 Hamilton, W.D. (1980) Oikos 35’. 282-290 6 Rice, W.R. (1983)Am. Nat. 121,187-203 7 Clay, K. (1984) NewPhytol. 98, 165-175 8 Kelley, S.E. and Clay, K. (1987) Evo/urion 41,92-l 03 9 Cheplick, G.P. and Clay, K. (1987)Am. J. Bat. 74,632 (abstract) 10 Alexander, H.M. (1987)Am. J. Bat. 74, 632 (abstract) 11 Parker, M.A. (1985) Evolution 39, 713-723 12 Parker, M.A. Heredity (in press) 13 Parker, M.A. (1987) Am. J. Bat. 74,633 (abstract) 14 Parker, M.A. Evolution (in press) 15 Parker, M.A. (1986) Oecologia 69, 253-259
In the next issue of TREE * The relationships of the major groups of mammals: new approaches, M . J. Benton * Are the pyramids deified dungpats? 1,Hanski * Tamarin and marmoset mating systems, A. Goldben * The adaptive significance of play, T. M . Care * Predation may link the cycles of lemmings and arctic birds, W . J. Sutherland 7