Effects of host plant and genetic background on the fitness costs of resistance to Bacillus thuringiensis

Novel resistance to pathogens and pesticides is commonly associated with a fitness cost. However, measurements of the fitness costs of insecticide resistance have used diverse methods to control for genetic background and rarely assess the effects of environmental variation. Here, we explored how genetic background interacts with resource quality to affect the expression of the fitness costs associated with resistance. We used a serially backcrossed line of the diamondback moth, Plutella xylostella, resistant to the biopesticide Bacillus thuringiensis, to estimate the costs of resistance for insects feeding on two Brassica species. We found that fitness costs increased on the better-defended Brassica oleracea cultivars. These data were included in two meta-analyses of fitness cost experiments that used standardized protocols (and a common resistant insect stock) but which varied in the methodology used to control for the effects of genetic background. The meta-analysis confirmed that fitness costs were higher on the low-quality host (B. oleracea); and experimental methodology did not influence estimates of fitness costs on that plant species. In contrast, fitness costs were heterogeneous in the Brassica pekinensis studies: fitness costs in genetically homogenized lines were significantly higher than in studies using revertant insects. We hypothesize that fitness modifiers can moderate fitness costs on high-quality plants but may not affect fitness when resource quality is low.     

Evolutionary rescue and adaptation to abrupt environmental change depends upon the history of stress

Whether evolution will be rapid enough to rescue declining populations will depend upon population size, the supply of genetic variation, the degree of maladaptation and the historical direction of selection. We examined whether the level of environmental stress experienced by a population prior to abrupt environmental change affects the probability of evolutionary rescue (ER). Hundreds of populations of two species of yeast, Saccharomyces cerevisiae and Saccharomyces paradoxus were exposed to a range of sublethal concentrations of salt for approximately a hundred generations before transfer to a concentration of salt lethal to the ancestor (150 g l^–1 NaCl). The fitness of surviving populations of both species was a quadratic function of yield: fitness was greatest for large populations that had been selected on low salt concentrations (less than 20 g l⁻¹ NaCl) and small populations that had adapted to high salt (more than 80 g l⁻¹ NaCl). However, differences occurred between species in the probability of ER. The frequency of ER was positively correlated with salt concentration for S. cerevisiae, but negatively correlated with salt concentration in S. paradoxus. These results not only demonstrate that past environmental conditions can determine the probability of ER after abrupt environmental change, but also suggest that there may even be differences between closely related species that are worth further exploration.     

The costs of evolving resistance in heterogeneous parasite environments

The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.     

A killer-rescue system for self-limiting gene drive of anti-pathogen constructs

A number of genetic mechanisms have been suggested for driving anti-pathogen genes into natural populations. Each of these mechanisms requires complex genetic engineering, and most are theoretically expected to permanently spread throughout the target species' geographical range. In the near term, risk issues and technical limits of molecular methods could delay the development and use of these mechanisms. We propose a gene-drive mechanism that can be self-limiting over time and space, and is simpler to build. This mechanism involves one gene that codes for toxicity (killer) and a second that confers immunity to the toxic effects (rescue). We use population-genetic models to explore cases with one or two independent insertions of the killer gene and one insertion of the rescue gene. We vary the dominance and penetrance of gene action, as well as the magnitude of fitness costs. Even with the fitness costs of 10 per cent for each gene, the proportion of mosquitoes expected to transmit the pathogen decreases below 5 per cent for over 40 generations after one 2:1 release (engineered:wild) or after four 1:2 releases. Both the killer and rescue genes will be lost from the population over time, if the rescue construct has any associated fitness cost. Molecular approaches for constructing strains are discussed.     

The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria

Background and Aims

Inbreeding via self-fertilization may have negative effects on plant fitness (i.e. inbreeding depression). Outbreeding, or cross-fertilization between genetically dissimilar parental plants, may also disrupt local adaptation or allelic co-adaptation in the offspring and again lead to reduced plant fitness (i.e. outbreeding depression). Inbreeding and outbreeding may also increase plant vulnerability to natural enemies by altering plant quality or defence. The effects of inbreeding and outbreeding on plant size and response to herbivory in the perennial herb, Vincetoxicum hirundinaria, were investigated.

Methods

Greenhouse experiments were conducted using inbred and outbred (within- and between-population) offspring of 20 maternal plants from four different populations, quantifying plant germination, size, resistance against the specialist folivore, Abrostola asclepiadis, and tolerance of simulated defoliation.

Key Results

Selfed plants were smaller and more susceptible to damage by A. asclepiadis than outcrossed plants. However, herbivore biomass on selfed and outcrossed plants did not differ. The effects of inbreeding on plant performance and resistance did not differ among plant populations or families, and no inbreeding depression at all was found in tolerance of defoliation. Between-population outcrossing had no effect on plant performance or resistance against A. asclepiadis, indicating a lack of outbreeding depression.

Conclusions

Since inbreeding depression negatively affects plant size and herbivore resistance, inbreeding may modify the evolution of the interaction between V. hirundinaria and its specialist folivore. The results further suggest that herbivory may contribute to the maintenance of a mixed mating system of the host plants by selecting for outcrossing and reduced susceptibility to herbivore attack, and thus add to the growing body of evidence on the effects of inbreeding on the mating system evolution of the host plants and the dynamics of plant–herbivore interactions.     

Changes in fitness-associated traits due to the stacking of transgenic glyphosate resistance and insect resistance in Brassica napus L

Increasingly, genetically modified crops are being developed to express multiple 'stacked' traits for different types of transgenes, for example, herbicide resistance, insect resistance, crop quality and tolerance to environmental stresses. The release of crops that express multiple traits could result in ecological changes in weedy environments if feral crop plants or hybrids formed with compatible weeds results in more competitive plants outside of agriculture. To examine the effects of combining transgenes, we developed a stacked line of canola (Brassica napus L.) from a segregating F(2) population that expresses both transgenic glyphosate resistance (CP4 EPSPS) and lepidopteran insect resistance (Cry1Ac). Fitness-associated traits were evaluated between this stacked genotype and five other Brassica genotypes in constructed mesocosm plant communities exposed to insect herbivores (Plutella xylostella L.) or glyphosate-drift. Vegetative biomass, seed production and relative fecundity were all reduced in stacked trait plants when compared with non-transgenic plants in control treatments, indicating potential costs of expressing multiple transgenes without selection pressure. Although costs of the transgenes were offset by selective treatment, the stacked genotype continued to produce fewer seeds than either single transgenic line. However, the increase in fitness of the stacked genotype under selective pressure contributed to an increased number of seeds within the mesocosm community carrying unselected, hitchhiking transgenes. These results demonstrate that the stacking of these transgenes in canola results in fitness costs and benefits that are dependent on the type and strength of selection pressure, and could also contribute to changes in plant communities through hitchhiking of unselected traits.     

Direct and ecological costs of resistance and tolerance in the stinging nettle

Plant resistance and tolerance to herbivores, parasites, pathogens, and abiotic factors may involve two types of costs. First, resistance and tolerance may be costly in terms of plant fitness. Second, resistance and tolerance to multiple enemies may involve ecological trade-offs. Our study species, the stinging nettle ( Urtica dioica L.) has significant variation among seed families in resistance and tolerance as well as costs of resistance and tolerance to the holoparasitic plant Cuscuta europaea L. Here we report on variation among seed families (i.e. genetic) in tolerance to nutrient limitation and in resistance to both mammalian herbivores (i.e. number of stinging trichomes) and an invertebrate herbivore (i.e. inverse of the performance of a generalist snail, Arianta arbustorum). Our results indicate direct fitness costs of snail resistance in terms of host reproduction whereas we did not detect fitness costs of mammalian resistance or tolerance to nutrient limitation. We further tested for ecological trade-offs among tolerance or resistance to the parasitic plant, herbivore resistance, and tolerance to nutrient limitation in the stinging nettle. Tolerance of nettles to nutrient limitation and resistance to mammalian herbivores tended to correlate negatively. However, there were no significant correlations among resistance and tolerance to the different natural enemies (i.e. parasitic plants, snails, and mammals). The results of this greenhouse study thus suggest that resistance and tolerance of nettles to diverse enemies are free to evolve independently of each other but not completely without direct costs in terms of plant fitness.     

Divergent selection along climatic gradients in a rare central European endemic species,Saxifraga sponhemica

Background and Aims The effects of habitat fragmentation on quantitative genetic variation in plant populations are still poorly known. Saxifraga sponhemica is a rare endemic of Central Europe with a disjunct distribution, and a stable and specialized habitat of treeless screes and cliffs. This study therefore used S. sponhemica as a model species to compare quantitative and molecular variation in order to explore (1) the relative importance of drift and selection in shaping the distribution of quantitative genetic variation along climatic gradients; (2) the relationship between plant fitness, quantitative genetic variation, molecular genetic variation and population size; and (3) the relationship between the differentiation of a trait among populations and its evolvability.Methods Genetic variation within and among 22 populations from the whole distribution area of S. sponhemica was studied using RAPD (random amplified polymorphic DNA) markers, and climatic variables were obtained for each site. Seeds were collected from each population and germinated, and seedlings were transplanted into a common garden for determination of variation in plant traits.Key Results In contrast to previous results from rare plant species, strong evidence was found for divergent selection. Most population trait means of S. sponhemica were significantly related to climate gradients, indicating adaptation. Quantitative genetic differentiation increased with geographical distance, even when neutral molecular divergence was controlled for, and Q_ST exceeded F_ST for some traits. The evolvability of traits was negatively correlated with the degree of differentiation among populations (Q_ST), i.e. traits under strong selection showed little genetic variation within populations. The evolutionary potential of a population was not related to its size, the performance of the population or its neutral genetic diversity. However, performance in the common garden was lower for plants from populations with reduced molecular genetic variation, suggesting inbreeding depression due to genetic erosion.Conclusions The findings suggest that studies of molecular and quantitative genetic variation may provide complementary insights important for the conservation of rare species. The strong differentiation of quantitative traits among populations shows that selection can be an important force for structuring variation in evolutionarily important traits even for rare endemic species restricted to very specific habitats.     

Problems and Strategies Associated with Long-term Use of Nematode Resistant Cultivars

Plant-parasitic nematodes are obligate parasites, and planting cultivars that are highly resistant to these organisms places extensive selection pressure on the target species and affects nontarget nematodes as well. Problems encountered with long-term planting of cultivars resistant to nematodes include shifts in nematode races or species and the occurrence of multiple species of nematodes within the same field. These problems can be alleviated to some extent when crop management is used to lessen the selection pressure for change on the nematode populations. Race shifts within populations and possibly shifts between nematode species can be delayed by rotating susceptible cultivars and nonhost crops with resistant cultivars. Nematicides in conjunction with resistant cultivars may be used to limit damage by multiple species of nematodes. Some cultivars have resistance to multiple species of nematodes, but greatly increased research effort is needed in this area. More intensive plant breeding effort will be required to make nematode resistant cultivars competitive in quality and yield with more productive, susceptible cultivars.     

A population of sexual Daphnia pulex resists invasion by asexual clones

Asexual reproduction avoids the costs associated with sex, predicting that invading asexual clones can quickly replace sexual populations. Daphnia pulex populations in the Great Lakes area are predominately asexual, but the elimination of sexual populations by invading clones is poorly understood. Asexual clones were detected at low frequency in one rare sexual population in 1995, with some increase in frequency during 2003 and 2004. However, these clones remained at low frequency during further yearly sampling (2005–2013) with no evidence that the resident sexual population was in danger of elimination. There was evidence for hybridization between rare males produced by asexual clones and sexual females with the potential to produce new asexual genotypes and spread the genetic factors for asexuality. In a short-term laboratory competition experiment, the two most common asexual clones did not increase in frequency relative to a genetically diverse sexual population due in part to a greater investment in diapausing eggs that trades-off current population growth for increased contribution to the egg bank. Our results suggest that a successful invasion can be prolonged, requiring a combination of clonal genotypes with high fitness, persistence of clones in the egg bank and negative factors affecting the sexual population such as inbreeding depression resulting from population bottlenecks.     

The Effects of Root-knot Nematode Infection and Mi-mediated Nematode Resistance in Tomato on Plant Fitness

The Mi-1.2 resistance gene in tomato (Solanum lycopersicum) confers resistance against several species of root-knot nematodes (Meloidogyne spp.). This study examined the impact of M. javanica on the reproductive fitness of near-isogenic tomato cultivars with and without Mi-1.2 under field and greenhouse conditions. Surprisingly, neither nematode inoculation or host plant resistance impacted the yield of mature fruits in field microplots (inoculum=8,000 eggs/plant), or fruit or seed production in a follow-up greenhouse bioassay conducted with a higher inoculum level (20,000 eggs/plant). However, under heavy nematode pressure (200,000 eggs/plant), greenhouse-grown plants carrying Mi-1.2 had more than ten-fold greater fruit production than susceptible plants and nearly forty-fold greater estimated lifetime seed production, confirming prior reports of the benefits of Mi-1.2. In all cases Mi-mediated resistance significantly reduced nematode reproduction. These results indicated that tomato can utilize tolerance mechanisms to compensate for moderate levels of nematode infection, but that the Mi-1.2 resistance gene confers a dramatic fitness benefit under heavy nematode pressure. No significant cost of resistance was detected in the absence of nematode infection.     

Induced Resistance to Meloidogyne hapla by other Meloidogyne species on Tomato and Pyrethrum Plants

Advance inoculation of the tomato cv. Celebrity or the pyrethrum clone 223 with host-incompatible Meloidogyne incognita or M. javanica elicited induced resistance to host-compatible M. hapla in pot and field experiments. Induced resistance increased with the length of the time between inoculations and with the population density of the induction inoculum. Optimum interval before challenge inoculation, or population density of inoculum for inducing resistance, was 10 days, or 5,000 infective nematodes per 500-cm³ pot. The induced resistance suppressed population increase of M. hapla by 84% on potted tomato, 72% on potted pyrethrum, and 55% on field-grown pyrethrum seedlings, relative to unprotected treatments. Pyrethrum seedlings inoculated with M. javanica 10 days before infection with M. hapla were not stunted, whereas those that did not receive the advance inoculum were stunted 33% in pots and 36% in field plots. The results indicated that advance infection of plants with incompatible or mildly virulent nematode species induced resistance to normally compatible nematodes and that the induced resistance response may have potential as a biological control method for plant nematodes.     

Experimental test for adaptive differentiation of ginseng populations reveals complex response to temperature

Background and Aims Local climatic adaptation can influence species' response to climate change. If populations within a species are adapted to local climate, directional change away from mean climatic conditions may negatively affect fitness of populations throughout the species' range. Methods Adaptive differentiation to temperature was tested for in American ginseng (Panax quinquefolius) by reciprocally transplanting individuals from two populations, originating at different elevations, among temperature treatments in a controlled growth chamber environment. Fitness-related traits were measured in order to test for a population × temperature treatment interaction, and key physiological and phenological traits were measured to explain population differences in response to temperature. Key Results Response to temperature treatments differed between populations, suggesting genetic differentiation of populations. However, the pattern of response of fitness-related variables generally did not suggest 'home temperature' advantage, as would be expected if populations were locally adapted to temperature alone. Conclusions Failure consistently to detect a 'home temperature' advantage response suggests that adaptation to temperature is complex, and environmental and biotic factors that naturally covary with temperature in the field may be critical to understanding the nature of adaptation to temperature.     

Population dynamics of defensive symbionts in aphids

Vertically transmitted micro-organisms can increase in frequency in host populations by providing net benefits to hosts. While laboratory studies have identified diverse beneficial effects conferred by inherited symbionts of insects, they have not explicitly examined the population dynamics of mutualist symbiont infection within populations. In the pea aphid, Acyrthosiphon pisum, the inherited facultative symbiont, Hamiltonella defensa, provides protection against parasitism by the wasp, Aphidius ervi. Despite a high fidelity of vertical transmission and direct benefits of infection accruing to parasitized aphids, Hamiltonella remains only at intermediate frequencies in natural populations. Here, we conducted population cage experiments to monitor the dynamics of Hamiltonella and of another common A. pisum symbiont, Serratia symbiotica, in the presence and absence of parasitism. We also conducted fitness assays of Hamiltonella-infected aphids to search for costs to infection in the absence of parasitism. In the population cages, we found that the frequency of A. pisum infected with Hamiltonella increased dramatically after repeated exposure to parasitism by A. ervi, indicating that selection pressures from natural enemies can lead to the increase of particular inherited symbionts in insect populations. In our laboratory fitness assays, we did not detect a cost to infection with Hamiltonella, but in the population cages not exposed to parasitism, we found a significant decline in the frequency of both Hamiltonella and Serratia. The declining frequencies of Hamiltonella-infected aphids in population cages in the absence of parasitism indicate a probable cost to infection and may explain why Hamiltonella remains at intermediate frequencies in natural populations.     

Forest fragmentation and plant reproductive success: a case study in four perennial herbs

We assessed the effects of habitat fragmentation on reproductive success in natural populations of four forest herbs with differing life-history traits and whose distribution patterns appeared to be negatively affected by decreased habitat size and/or increased isolation: Carex sylvatica, Galium odoratum, Sanicula europaea and Veronica montana. Our aims were to test (1) whether habitat size and isolation are positively correlated with population size and isolation, respectively, (2) whether plant reproductive success, a major component of plant fitness, is reduced in small and/or isolated populations when also accounting for differences in habitat quality (edaphic conditions, light intensity) and the effects of plant size, and (3) whether species with different life histories are affected differently. There were significant positive relationships between habitat and population size and between habitat and population isolation in some, but not all of the species. We mostly found no negative effects of small population size or isolation on reproduction. However, reproductive success was reduced in small populations of Sanicula, and this effect was independent of differences in plant size and environmental conditions. The reduced fecundity in small populations may be a consequence of the Allee-effect, a possible mechanism being pollen limitation. Furthermore, the proportion of flowering ramets was reduced in small and isolated populations of Galium, which may have been caused by changes in population structure. Lastly, we found some evidence for largely outcrossing, non-clonal species to be more sensitive to reductions in population size, at least in terms of their reproductive success.     

Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress

Parental effort is usually associated with high metabolism that could lead to an increase in the production of reactive oxidative species giving rise to oxidative stress. Since many antioxidants involved in the resistance to oxidative stress can also enhance immune function, an increase in parental effort may diminish the level of antioxidants otherwise involved in parasite resistance. In the present study, we performed brood size manipulation in a population of great tits (Parus major) to create different levels of parental effort. We measured resistance to oxidative stress and used a newly developed quantitative PCR assay to quantify malarial parasitaemia. We found that males with an enlarged brood had significantly higher level of malarial parasites and lower red blood cell resistance to free radicals than males rearing control and reduced broods. Brood size manipulation did not affect female parasitaemia, although females with an enlarged brood had lower red blood cell resistance than females with control and reduced broods. However, for both sexes, there was no relationship between the level of parasitaemia and resistance to oxidative stress, suggesting a twofold cost of reproduction. Our results thus suggest the presence of two proximate and independent mechanisms for the well-documented trade-off between current reproductive effort and parental survival.     

Population divergence and gene flow in an endangered and highly mobile seabird

Seabirds are highly vagile and can disperse up to thousands of kilometers, making it difficult to identify the factors that promote isolation between populations. The endemic Hawaiian petrel (Pterodroma sandwichensis) is one such species. Today it is endangered, and known to breed only on the islands of Hawaii, Maui, Lanai and Kauai. Historical records indicate that a large population formerly bred on Molokai as well, but this population has recently been extirpated. Given the great dispersal potential of these petrels, it remains unclear if populations are genetically distinct and which factors may contribute to isolation between them. We sampled petrels from across their range, including individuals from the presumably extirpated Molokai population. We sequenced 524 bp of mitochondrial DNA, 741 bp from three nuclear introns, and genotyped 18 microsatellite loci in order to examine the patterns of divergence in this species and to investigate the potential underlying mechanisms. Both mitochondrial and nuclear data sets indicated significant genetic differentiation among all modern populations, but no differentiation was found between historic samples from Molokai and modern birds from Lanai. Population-specific nonbreeding distribution and strong natal philopatry may reduce gene flow between populations. However, the lack of population structure between extirpated Molokai birds and modern birds on Lanai indicates that there was substantial gene flow between these populations and that petrels may be able to overcome barriers to dispersal prior to complete extirpation. Hawaiian petrel populations could be considered distinct management units, however, the dwindling population on Hawaii may require translocation to prevent extirpation in the near future.     

Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm

Fitness costs associated with insect resistance to Bacillus thuringiensis (Bt) crops may help to delay or prevent the spread of resistance alleles, especially when refuges of non-Bt host plants are present. The potential for such delays increases as the magnitude and dominance of fitness costs increase. Here, we examined the idea that plant secondary chemicals affect expression of fitness costs associated with resistance to Bt cotton in Pectinophora gossypiella (Saunders). Specifically, we tested the hypotheses that gossypol affects the magnitude or dominance of fitness costs, by measuring performance of three independent sets of pink bollworm populations fed artificial diet with and without gossypol. Each set had an unselected susceptible population, a resistant population derived by selection from the susceptible population, and the F1 progeny of the susceptible and resistant populations. No individuals completed development on diets with gossypol in one set, suggesting that these individuals partially lost the ability to detoxify this chemical. In the other two sets, costs affecting survival did not support the hypotheses, but costs affecting pupal weight did. Adding gossypol to diet increased the magnitude and dominance of costs affecting pupal weight. In one of the two sets with survivors on diet with gossypol, costs affecting development time were less recessive when gossypol was present in diet. These results indicate that gossypol increased the magnitude and dominance of some fitness costs. Better understanding of the effects of natural plant defenses on fitness costs could improve our ability to design refuges for managing insect resistance to Bt crops.     

Phenotypic plasticity as an index of drought tolerance in three Patagonian steppe grasses

Background and Aims

Despite general agreement regarding the adaptive importance of plasticity, evidence for the role of environmental resource availability in plants is scarce. In arid and semi-arid environments, the persistence and dominance of perennial species depends on their capacity to tolerate drought: tolerance could be given on one extreme by fixed traits and, on the other, by plastic traits. To understand drought tolerance of species it is necessary to know the plasticity of their water economy-related traits, i.e. the position in the fixed–plastic continuum.

Methods

Three conspicuous co-existing perennial grasses from a Patagonian steppe were grown under controlled conditions with four levels of steady-state water availability. Evaluated traits were divided into two groups. The first was associated with potential plant performance and correlated with fitness, and included above-ground biomass, total biomass, tillering and tiller density at harvest. The second group consisted of traits associated with mechanisms of plant adjustment to environmental changes and included root biomass, shoot/root ratio, tiller biomass, length of total elongated leaf, length of yellow tissue divided by time and final length divided by the time taken to reach final length.

Key Results and Conclusions

The most plastic species along this drought gradient was the most sensitive to drought, whereas the least plastic and slowest growing was the most tolerant. This negative relationship between tolerance and plasticity was true for fitness-related traits but was trait-dependent for underlying traits. Remarkably, the most tolerant species had the highest positive plasticity (i.e. opposite to the default response to stress) in an underlying trait, directly explaining its drought resistance: it increased absolute root biomass. The niche differentiation axis that allows the coexistence of species in this group of perennial dryland grasses, all limited by soil surface moisture, would be a functional one of fixed versus plastic responses.     

Cost of resistance and tolerance under competition: the defense-stress benefit hypothesis

Defense costs provide a major explanation for why plants in nature have not evolved to be better defended against pathogens and herbivores; however, evidence for defense costs is often lacking. Plants defend by deploying resistance traits that reduce damage, and tolerance traits that reduce the fitness effects of damage. We first tested the defense-stress cost (DSC) hypothesis that costs of defenses increase and become important under competitive stress. In a greenhouse experiment, uniparental maternal families of the host plant Arabis perennans were grown in the presence and absence of the bunch grass Bouteloua gracilis and the herbivore Plutella xylostella. Costs of resistance and tolerance manifest as reduced growth in the absence of herbivory were significant when A. perennans grew alone, but not in the competitive environment, in contrast to the DSC hypothesis. We then tested the defense-stress benefit (DSB) hypothesis that plant defenses may benefit plants in competitive situations thereby reducing net costs. For example, chemical resistance agents and tolerance may also have functions in competitive interactions. To test the DSB hypothesis, we compared differentially competitive populations for defense costs, assuming that poorer competitors from less dense habitats were less likely to have evolved defenses that also function in competition. Without competitive benefits of defenses, poorer competitors were expected to have higher net costs of defenses under competition in accordance with DSB. Populations of A. perennans and A. drummondii that differed dramatically in competitiveness were compared for costs, and as the DSB hypothesis predicts, only the poor competitor population showed costs of resistance under competition. However, cost of tolerance under competition did not differ among populations, suggesting that the poor competitors might have evolved a general stress tolerance. Although the DSC hypothesis may explain cases where defense costs increase under stress, the DSB hypothesis may explain some cases where costs decrease under competitive stress.