Does the Cost of Adaptation to Extremely Stressful Environments Diminish Over Time? A Literature Synthesis on How Plants Adapt to Heavy Metals and Pesticides

Populations adapted to locally stressful environmental conditions are predicted to carry costs in performance and fitness, particularly when compared to non-stress adapted populations in the absence of stress. However, empirical observations found fitness costs incurred by stress-resistant genotypes are often ambiguous or absent. Compensatory evolution may purge genotypes with relatively high costs over time, resulting in the recovery of fitness in a stress-resistant population. We assessed the magnitude of adaptation costs over time to test for a reduction in negative genetic effects by compiling published data on measures of fitness from plant populations inhabiting mine tailings and populations adapted to herbicides. Heavy metal contaminated sites represent a stress that is immediate and unchanging; herbicides represent a stress that changes over time with dosage or the type of herbicide as treated populations become more resistant. To quantify costs, for each comparison we recorded the performance of plants from stress and non-stress environments grown under benign conditions. Time since the initiation of the stress was determined to test whether costs change over time. Costs were overall constant through time. The magnitude of cost were consistent with trade-offs for heavy metal resistance and certain herbicide mechanisms (triazine and resistance via P450 enzyme), but not for other herbicides where costs were inconsistent and appear to be low if not absent. Superior stress-resistant populations with higher performance than non-stress populations were found from both herbicide and metal stress, with some extreme cases early from time since initiation. There was an increasing benefit to cost ratio over time for herbicide resistant populations. We found that adaptation to stressful environments is generally costly except in herbicide resistance, and that costs are not diminished over time. Stress-resistant populations without costs also arise infrequently, though these populations may often be restricted from spreading.     

GENETICS OF BRASSICA RAPA. 3. COSTS OF DISEASE RESISTANCE TO THREE FUNGAL PATHOGENS

Genetic costs of resistance to pathogens may be an important factor maintaining heritable variation for resistance in natural populations. Pleiotropic fitness trade-offs occur when genetic resistance causes reduction in other components of fitness. Although costs of resistance have an important influence on plant-pathogen interactions, few previous studies have detected pleiotropic costs of resistance in the absence of confounding effects of linkage disequilibrium. To avoid this potential problem, we performed artificial selection experiments on resistance to two fungal pathogens, Leptosphaeria maculans, and Peronospora parasitica, and compared growth rates of resistant and susceptible genotypes of Brassica rapa in the absence of pathogens. Leptosphaeria resistance had no effect on growth rate, indicating cost-free defense. In contrast, Peronospora-resistant genotypes grow 6% slower than Peronospora-susceptible genotypes in pathogen-free environments, indicating a significant genetic fitness cost to Peronospora resistance. Such genetic trade-offs could maintain genetic variation in the wild. Another factor that might explain heritable variation for resistance is ecological trade-offs, in which genetic resistance to one species causes susceptibility to another. Such ecological trade-offs do not exist for the pathogens studied in this system.     

The experimental evolution of herbicide resistance in Chlamydomonas reinhardtii results in a positive correlation between fitness in the presence and absence of herbicides

Pleiotropic fitness trade-offs will be key determinants of the evolutionary dynamics of selection for pesticide resistance. However, for herbicide resistance, empirical support for a fitness cost of resistance is mixed, and it is therefore also questionable what further ecological trade-offs can be assumed to apply to herbicide resistance. Here, we test the existence of trade-offs by experimentally evolving herbicide resistance in Chlamydomonas reinhardtii. Although fitness costs are detected for all herbicides, we find that, counterintuitively, the most resistant populations also have the lowest fitness costs as measured by growth rate in the ancestral environment. Furthermore, after controlling for differences in the evolutionary dynamics of resistance to different herbicides, we also detect significant positive correlations between resistance, fitness in the ancestral environment and cross-resistance to other herbicides. We attribute this to the highest levels of nontarget-site resistance being achieved by fixing mutations that more broadly affect cellular physiology, which results in both more cross-resistance and less overall antagonistic pleiotropy on maximum growth rate. Consequently, the lack of classical ecological trade-offs could present a major challenge for herbicide resistance management.     

Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off

Trade-offs can maintain genetic diversity and constrain adaptation; however, their magnitude may depend on ecological factors. I considered whether resistance to the herbicide triazine in Amaranthus hybridus (Amaranthaceae) imposed the trade-off of increasing susceptibility to herbivorous insects. I grew triazine-resistant and triazine-susceptible plants under contrasting levels of light and fertilization, and quantified susceptibility to herbivores using the specialist Disonycha glabrata (Coleoptera: Chrysomelidae) and the generalist Trichoplusia ni (Lepidoptera: Noctuidae). Resistance to triazine increased susceptibility to both species of herbivorous insects, as manifested by greater feeding preference, growth, and survival of herbivores. However, these effects were more pronounced with T. ni and for plants grown under high light. My results demonstrate the presence of a trade-off between resistance to triazine and susceptibility to herbivorous insects that may in turn impose an ecologically based fitness cost, and illustrate the potential for this cost to vary across environments.     

Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus

Directional selection for plant traits associated with resistance to herbivory tends to eliminate genetic variation in such traits. On the other hand, balancing selection arising from trade-offs between resistance and growth or spatially variable selection acts against the elimination of genetic variation. We explore both the amount of genetic variation and variability of natural selection for growth and concentration of phenolic secondary compounds, phlorotannins, in the brown alga Fucus vesiculosus. We measured variation in selection at two growing depths and two levels of nutrient availability in algae that had faced two kinds of past growing environments. Genetic variation was low for growth but high for phlorotannins. The form and strength of selection for both focal traits depended on the past growing environment of the algae. We found strong directional selection for growth rate in algae previously subjected to higher ultraviolet radiation, but not in algae previously subjected to higher nutrient availability. Stabilizing selection for growth occurred especially in the deep growing environment. Selection for phlorotannins was generally weak, but in some past-environment-current-environment combinations we detected either directional selection against phlorotannins or stabilizing selection. Thus, phlorotannins are not selectively neutral but affect the fitness of F. vesiculosus. In particular, there may be a fitness cost of producing phlorotannins, but the realization of such a cost varies from one environment to another. Genetic correlations between selective environments were high for growth but nonexistent for phlorotannins, emphasizing the high phenotypic plasticity of phlorotannin production. The highly heterogeneous selection, including directional, stabilizing, and spatially variable selection as well as temporal change in selection due to responses to past environmental conditions, probably maintains a high amount of genetic variation in phlorotannins. Such variation provides the potential for rapid evolutionary response of phlorotannins under directional selection.     

CLONAL VARIATION AND COVARIATION IN APHID RESISTANCE TO PARASITOIDS AND A PATHOGEN

Abstract The potential rate of evolution of resistance to natural enemies depends on the genetic variation present in the population and any trade-offs between resistance and other components of fitness. We measured clonal variation and covariation in pea aphids ( Acyrthosiphon pisum ) for resistance to two parasitoid species ( Aphidius ervi and A. eadyi ) and a fungal pathogen ( Erynia neoaphidis ). We found significant clonal variation in resistance to all three natural enemies. We tested the hypothesis that there might be trade-offs (negative covariation) in defensive ability against different natural enemies, but found no evidence for this. All correlations in defensive ability were positive, that between the two parasitoid species significantly so. Defensive ability was not correlated with fecundity. A number of aphid clones were completely resistant to one parasitoid ( A. eadyi ), but a subset of these failed to reproduce subsequently. We discuss the factors that might maintain clonal variation in natural enemy resistance.     

Costs of herbivore resistance in clonal saplings of <Emphasis Type="Italic">Betula pendula</Emphasis>

Several studies have found genetic variation in plant resistance to herbivory. One of the explanations suggested for the observed intermediate levels of resistance are the costs of resistance, i.e., negative genetic correlations between resistance and other fitness components that may constrain the evolution of resistance. We studied the cost of herbivore resistance by investigating the genetic correlations between resistance traits and plant growth traits, and between resistance to insect and mammalian herbivores in cloned saplings of silver birch, Betula pendula. We used the performance of a geometrid moth, Epirrita autumnata, as an indicator of insect resistance. The numbers of resin droplets at the base and at the tip of the saplings correlate with mammalian resistance, and were thus used here as indicators of vole and hare resistance, respectively. We have previously observed genetic variation in these resistance traits. Further, we examined the correlations between several groups of secondary chemicals and plant growth traits. Finally, to reveal the effect of environmental factors on the trade-offs mentioned above, we investigated the correlations in saplings that were grown at two nutrient levels. We found significant negative correlations between indices of constitutive insect resistance and relative height growth in non-fertilized saplings, indicating cost of constitutive insect resistance. The two groups of secondary chemicals that have been shown to correlate strongly with constitutive insect resistance, i.e., condensed tannins and flavonol glycosides (especially myricetin glycosides), had different genetic correlations with plant traits; the concentration of condensed tannins did not correlate negatively with any of the plant traits, whereas the concentration of flavonol glycosides correlated negatively with plant height. Insect and mammalian resistance did not correlate negatively, indicating no ecological trade-offs.     

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.     

Biorational management tactics to select against triazine-resistant Amaranthus hybridus: a field trial

1. The individual and joint effectiveness of two biorational tactics (crop interference and exploitation of negative cross-resistance to certain herbicides) in the management of triazine-resistant Amaranthus hybridus L. (smooth pigweed) were estimated. Biorational tactics exploit biological idiosyncracies of resistant (R) genotypes to maximize fitness cost(s) of resistance. We quantified selection against triazine resistance by relative performance comparisons between lines having comparable nuclear genomes but either resistant or susceptible cytoplasm. Increasing soybean density by reducing row spacing (from 76 cm to 25 cm) did not significantly increase the fitness cost of resistance.
2. Low doses of bentazon (100 and 300 g active ingredient ha^–1) did strongly increase the cost of resistance. Over 2 years, the mean relative performance of R genotypes in bentazon treatments was 0·40, compared to 0·60 in the absence of bentazon. Therefore, use of bentazon in soybean production has the potential to delay evolution of triazine resistance in maize–soybean rotations using triazines.
3. There was no consistent indication that increased soybean density and bentazon herbicide could act synergistically to increase costs of triazine resistance in Amaranthus hybridus . Nor were differences in response to biorational tactics evident between the two populations of origin (Maryland and Virginia, USA) from which experimental lines were derived.
4. Effects of the biorational tactics differed markedly between years, highlighting that resistance management depending primarily on these tactics would have widely variable results. Use of such tactics is likely to be most effective in the context of diversified weed management.     

Effects of Cu/Zn superoxide dismutase (sod1) genotype and genetic background on growth, reproduction and defense in Biomphalaria glabrata

Resistance of the snail Biomphalaria glabrata to the trematode Schistosoma mansoni is correlated with allelic variation at copper-zinc superoxide dismutase (sod1). We tested whether there is a fitness cost associated with carrying the most resistant allele in three outbred laboratory populations of snails. These three populations were derived from the same base population, but differed in average resistance. Under controlled laboratory conditions we found no cost of carrying the most resistant allele in terms of fecundity, and a possible advantage in terms of growth and mortality. These results suggest that it might be possible to drive resistant alleles of sod1 into natural populations of the snail vector for the purpose of controlling transmission of S. mansoni. However, we did observe a strong effect of genetic background on the association between sod1 genotype and resistance. sod1 genotype explained substantial variance in resistance among individuals in the most resistant genetic background, but had little effect in the least resistant genetic background. Thus, epistatic interactions with other loci may be as important a consideration as costs of resistance in the use of sod1 for vector manipulation.     

On the transfer of fitness from the cell to the multicellular organism

The fitness of any evolutionary unit can be understood in terms of its two basic components: fecundity (reproduction) and viability (survival). Trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. We argue that these trade-offs gain special significance during the transition from unicellular to multicellular life. In particular, the evolution of germ–soma specialization and the emergence of individuality at the cell group (or organism) level are also consequences of trade-offs between the two basic fitness components, or so we argue using a multilevel selection approach. During the origin of multicellularity, we study how the group trade-offs between viability and fecundity are initially determined by the cell level trade-offs, but as the transition proceeds, the fitness trade-offs at the group level depart from those at the cell level. We predict that these trade-offs begin with concave curvature in single-celled organisms but become increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the cost of reproduction which increases as group size increases. We consider aspects of the biology of the volvocine green algae – which contain both unicellular and multicellular members – to illustrate the principles and conclusions discussed.     

Genetic variation in fitness parameters associated with resistance to Bacillus thuringiensis in male and female Trichoplusia ni

Resistance of insects to insecticides is often associated with reduced fitness in the absence of selection. We examined fitness trade-offs associated with resistance to the microbial insecticide, Bacillus thuringiensis (Bt), across full-sib families in a resistant population of Trichoplusia ni. Significant genetic variation in and heritability of susceptibility to Bt occurred among the full-sib families. Male pupal weight was positively correlated with Bt susceptibility, indicating a potential fitness cost, but no such correlation occurred for females. Significant heritability for pupal weight was present for males but not females. A significant negative genetic correlation existed between development time and Bt susceptibility, indicating that resistant larvae developed more slowly than susceptible larvae. Selection for Bt resistance in T. ni resulted in changes in life-history traits that affected males more than females.     

Quantitative evidence for early life fitness defects from 32 longevity-associated alleles in yeast

Reduced fecundity has been associated with some alleles that enhance longevity in invertebrate and mammalian models. This observation has been suggested to support the antagonistic pleiotropy theory of aging, which predicts that alleles of some genes promoting fitness early in life have detrimental effects later in life that limit survival. In only a few cases, however, has the relative fitness of long-lived mutants been quantified through direct competition with the wild type genotype. Here we report the first comprehensive analysis of longevity/fitness trade-offs by measuring the relative fitness of 49 long-lived yeast variants in a direct competition assay with wild type cells. We find that 32 (65%) of these variants show a significant defect in fitness in this competition assay. In 26 (81%) of these cases, this reduction in fitness can be partially accounted for by reduced maximal growth rate during early life, usually resulting from a G0/G1-specific cell cycle defect. A majority of the less fit longevity-enhancing variants are associated with reduced mRNA translation. These findings are therefore consistent with the idea that enhanced longevity often comes with a fitness cost and suggest that this cost is often associated with variation in a subset of longevity factors, such as those regulating mRNA translation, growth, and reproduction.     

Positive genetic correlations among major life-history traits related to ecological success in the aphid Myzus persicae

Life-history theory is based on the assumption that evolution is constrained by trade-offs among different traits that contribute to fitness. Such trade-offs should be evident from negative genetic correlations among major life-history traits. However, this expectation is not always met. Here I report the results of a life-table experiment designed to measure the broad-sense heritabilities of life-history traits and their genetic correlations in 19 different clones of the aphid Myzus persicae from Victoria, Australia. Most individual traits, as well as fitness calculated as the finite rate of increase from the life table, exhibited highly significant heritabilities. The pattern of genetic correlations revealed absolutely no evidence for life-history trade-offs. Rather, life histories were arranged along an axis from better to worse. Clones with shorter development times tended to have larger body sizes, higher fecundities, and larger offspring. The fitness of clones estimated from the life table in the laboratory tended to be positively associated with their abundance in the field. Fitness also increased significantly with heterozygosity at the seven microsatellite loci that were used to distinguish clones and estimate their frequencies in the field. I discuss these findings in light of a recent proposition that positive genetic correlations among life-history traits for which trade-offs are expected can be explained by genetic variation for resource acquisition ability that is maintained in populations by a cost of acquisition, and I propose ways to test for such a cost in M. persicae.     

Experimental evolution of ultraviolet radiation resistance in Escherichia coli

Ultraviolet (UV) light is a major cause of stress, mutation, and mortality in microorganisms, causing numerous forms of cellular damage. Nevertheless, there is tremendous variation within and among bacterial species in their sensitivity to UV light. We investigated direct and correlated responses to selection during exposure to UV. Replicate lines of Escherichia coli K12 were propagated for 600 generations, half with UV and half as a control without UV. All lines responded to selection, and we found strong positive and negative correlated responses to selection associated with increased UV resistance. Compared to Control populations, UV-selected populations increased in desiccation and starvation resistance approximately twofold but were 10 times more sensitive to hypersalinity. There was little evidence for a persistent large competitive fitness cost to UV resistance. These results suggest that natural variation in UV resistance may be maintained by trade-offs for resistance to other abiotic sources of mortality. We observed an average twofold increase in cell size by the UV-selected populations, consistent with a structural mode of adaptation to UV exposure having preadaptive and maladaptive consequences to other abiotic stresses.     

Trade-off between larval development rate and Post-metamorphic Traits in the Frog Rana latastei

Development rate early in the ontogeny is believed to correlate positively with fitness. Geographic variation in intrinsic development rate suggests the existence of trade-offs between development rate and other fitness related traits. We investigated whether these trade-offs exist between intrinsic larval development rate and post-metamorphic traits in an organism with a complex life cycle. In laboratory, we measured if the tadpoles of the frog Rana latastei with fast intrinsic development rate have a suboptimal post-metamorphic morphology, by comparing froglets from five populations. Then, we evaluated the relationship between age at metamorphosis, hindlimb length and jumping performance for frogs grown in nature in two populations. Under laboratory conditions, froglets with fast intrinsic development had shorter absolute and shorter size-adjusted tibiofibulas. We observed a strong, positive relationship between tibiofibula length and jumping performance. In nature, froglets from the last metamorphosing population had longer absolute and size-adjusted tibiofibulas, and were able to jump further. The cost of fast development could be the shorter legs of early metamorphosing frogs, and their poor jumping performance. Thus, a fast intrinsic development rate may not always be positively related to lifetime fitness, since delayed effects of larval development persist also across life history stages. Co-ordinating editor: V. Jormalainen     

Life-history evolution and the origin of multicellularity

The fitness of an evolutionary individual can be understood in terms of its two basic components: survival and reproduction. As embodied in current theory, trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. Here, we argue that the evolution of germ-soma specialization and the emergence of individuality at a new higher level during the transition from unicellular to multicellular organisms are also consequences of trade-offs between the two components of fitness-survival and reproduction. The models presented here explore fitness trade-offs at both the cell and group levels during the unicellular-multicellular transition. When the two components of fitness negatively covary at the lower level there is an enhanced fitness at the group level equal to the covariance of components at the lower level. We show that the group fitness trade-offs are initially determined by the cell level trade-offs. However, as the transition proceeds to multicellularity, the group level trade-offs depart from the cell level ones, because certain fitness advantages of cell specialization may be realized only by the group. The curvature of the trade-off between fitness components is a basic issue in life-history theory and we predict that this curvature is concave in single-celled organisms but becomes increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the initial cost of reproduction to survival which increases as group size increases. To illustrate the principles and conclusions of the model, we consider aspects of the biology of the volvocine green algae, which contain both unicellular and multicellular members.     

How might Gyrodactylus parasitism modify trade-offs between female preference and susceptibility of males to predation in Trinidadian guppies?

A number of examples exist of trade-offs between mating success and survival; that is, success in one fitness component comes at the cost of success in the other fitness component. However, these expected trade-offs are – perhaps even more commonly – not observed. One explanation for this apparent paradox of missing trade-offs could be that the other factors generating fitness variation across individuals confound or obscure the expected trade-off. These confounding effects could arise in two general ways: (i) the additional source of variation could positively (or negatively) influence both fitness components (“shared confounder” hypothesis), or (ii) the additional source of variation could influence only one fitness component (“non-shared confounder” hypothesis). We tested whether parasitism by Gyrodactylus spp. could be a confounder of trade-offs between female preference and susceptibility to predation for male Trinidadian guppies (Poecilia reticulata). As in previous work, we did not find the expected trade-off; that is, the males preferred by females were not more likely to be eaten by predators. Because half of the experimental males were infected by Gyrodactylus in a paired design, we were able to show that females discriminated against infected males, but that infected males were not more susceptible to predation. Our results thus provide support for the non-shared confounder hypothesis. That is, by negatively affecting one fitness component (female choice) but not the other (susceptibility to predation), parasitism by Gyrodactylus could obscure the expected trade-off between female preference and susceptibility to predation.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

THE EVOLUTION OF RESISTANCE TO HERBIVORY IN IPOMOEA PURPUREA. II. NATURAL SELECTION BY INSECTS AND COSTS OF RESISTANCE

An important component of the process of coevolution between plants and their insect herbivores is the imposition of selection on plants by insects. Although such selection has been inferred from indirect evidence, little direct evidence for it exists. One goal of this study was to seek direct evidence by determining, for a single plant-herbivore system, whether insect herbivores impose selection on their host plants. A second goal was to determine whether costs are associated with genotypes that confer resistance to herbivores, as has been commonly postulated. The annual morning glory, Ipomoea purpurea, exhibits genetic variation in resistance to four different types of insects. For three of these types, most of the genetic variation is additive. Removal of insect herbivores increased the number of seeds produced by I. purpurea by 20% and eliminated additive genetic variation for seed number (fitness). This result implies that herbivores impose selection on some trait(s) of their host plants. Coupled with selection for decreased damage by corn earworms, as revealed by a negative additive genetic covariance between damage and fitness, this result suggests that insect herbivores impose selection on resistance to corn earworms in I. purpurea. Two types of cost of resistance to herbivores were sought in I. purpurea: 1) internal trade-offs in allocation of resources and 2) ecological trade-offs between resistances to different insects. No costs of either type were detected. This result suggests that cost-benefit arguments that attempt to predict the evolution of levels of resistance to herbivores are not applicable to I. purpurea.