EVALUATING A HYPOTHESIS ABOUT HETEROCHRONY: LARVAL LIFE-HISTORY TRAITS AND JUVENILE HIND-LIMB MORPHOLOGY IN HYLA CRUCIFER

This paper reports the results of an investigation into whether selection on genetically based differences in the timing or rate of development (heterochrony) can give rise to nonadaptive morphological differences among individual frogs. We used a quantitative-genetics approach to examine the relationships among the life-history characters time to metamorphosis and larval-growth rate and a functionally significant morphological features, relative hind-limb length, in the spring peeper, Hyla crucifer. Time to metamorphosis and growth rate had low heritabilities in our population. Morphological traits had moderate heritabilities. There were positive genetic correlations between the life-history traits and the components of relative hind-limb length but no significant correlations with the shape variable itself. We used field observations of pond-drying time and experimental results of selection on growth rate to simulate the correlated responses of hind-limb shape to four reasonable selection regimes on the life-history traits. We found little evidence to suggest that relative hind-limb length would display much of a correlated response to such selection. The differences in relative hind-limb length seen among closely related species or among populations of a single species that appear to be unrelated to performance differences are not obviously explicable as neutral correlated responses to selection on larval traits.     

Ontogenetic plasticity of anatomical and ecophysiological traits and their correlations in Iris pumila plants grown in contrasting light conditions

To better understand what directs and limits the evolution of phenotype, constraints in the realization of the optimal phenotype need to be addressed. That includes estimations of variability of adaptively important traits as well as their correlation structures, but also evaluation of how they are affected by relevant environmental conditions and development phases. The aims of this study were to analyze phenotypic plasticity, genetic variability and correlation structures of important Iris pumila leaf traits in different light environments and ontogenetic phases, and estimate its evolutionary potential. Stomatal density, specific leaf area, total chlorophyll concentration and chlorophyll a/b ratio were analyzed on I. pumila full‐sib families in the seedling phase and on the same plants after 3 years of growth in contrasting light conditions typical for ontogenetic stage in question. There was a significant phenotypic plasticity in both ontogenetic stages, but significant genetic variability was detected only for chlorophyll concentrations. Correlations of the same trait between different stages were weak due to changes in environmental conditions and difference in ontogenetic reaction norms of different genotypes. Ontogenetic variability of correlation structures was detected, where correlations and integration were higher in seedlings compared with adult plants 3 years later. Correlations were affected by environmental conditions, with integration being higher in the lower light conditions, but correlations between phases being stronger in the higher light treatment. These findings demonstrated that the analyzed traits can be selected and can mostly evolve independently in different environments and ontogenetic stages, with low genetic variability as a potentially main constraint.     

Post-metamorphic change in activity metabolism of anurans in relation to life history

Summary Newly-metamorphosed individuals of some species of frogs and toads differ from adults in behavior, ecology, and physiology. These differences may be related to broader patterns of the life histories of different species of frogs. In particular, the length of larval life and the size of a frog at metamorphosis appear to be significant factors in post-metamorphic ontogenetic change. These changes in performance are associated with rapid post-metamorphic increases in oxygen transport capacity. Bufo americanus (American toads) and Rana sylvatica (wood frogs) spend only 2–3 months as tadpoles and metamorphose at body masses of 0.25 g or less. Individuals of these species improve endurance and aerobic capacity rapidly during the predispersal period immediately following metamorphosis. Increases in hematocrit, hemoglobin concentration, and heart mass relative to body mass are associated with this improvement in organismal performance. Rana clamitans (green frogs) spend from 3 to 10 months as larvae and weigh 3 g at metamorphosis. Green frogs did not show immediate post-metamorphic increases in performance. Rana palustris (pickerel frogs) are intermediate to wood frogs and green frogs in length of larval life and in size at metamorphosis, and they are intermediate also in their post-metamorphic physiological changes.American toads and wood frogs appear to delay dispersal from their natal ponds while they undergo rapid post-metamorphic growth and development, whereas green frogs disperse as soon as they leave the water, even before they have fully absorbed their tails. The very small body sizes of newly metamorphosed toads and wood frogs appear to limit the scope of their behaviors. The brief larval periods of these species permit them to exploit transient aquatic habitats, but impose costs in the form of a period of post-metamorphic life in which their activities are restricted in time and space compared to those of adults.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.     

A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the pacific tree frog, Hyla regilla

Metamorphosis is assumed to be beneficial because it can break developmental links between traits in the different phases of a complex life-cycle and thereby allow larval and adult phases to adapt independently. I tested the prediction that correlations between the larval and adult phases are smaller than within stages. I estimated phenotypic and additive genetic variances and correlations for tadpole swimming speed, frog jump distance, body size, and larval period in a single population of the Pacific tree frog, Hyla regilla. These traits are known or reasonably assumed to be important for survival in this and other anuran species from temporary ponds. Only the three size variables were affected by sire identity. Heritabilities for locomotor performance, larval period, and size-independent performance were low (0.00-0.23) and not significant. Body size measurements showed somewhat higher and statistically significant heritabilities (0.24-0.34). Most traits were phenotypically correlated. On average, phenotypic correlations were larger between phases than within phases (0.41 vs. 0.28). Genetic correlations involving body-size traits were positive and large, and average within- and between-phase genetic correlation coefficients were identical (0.81). These results do not support the adaptive decoupling hypothesis, and they indicate that a paucity of additive genetic variation is a likely constraint on the evolution of traits measured for this population.     

Mixed evidence for the erosion of intertactical genetic correlations through intralocus tactical conflict

Alternative reproductive tactics, whereby members of the same sex use different tactics to secure matings, are often associated with conditional intrasexual dimorphisms. Given the different selective pressures on males adopting each mating tactic, intrasexual dimorphism is more likely to arise if phenotypes are genetically uncoupled and free to evolve towards their phenotypic optima. However, in this context, genetic correlations between male morphs could result in intralocus tactical conflict (ITC). We investigated the genetic architecture of male dimorphism in bulb mites (Rhizoglyphus echinopus) and earwigs (Forficula auricularia). We used half‐sibling breeding designs to assess the heritability and intra/intersexual genetic correlations of dimorphic and monomorphic traits in each species. We found two contrasting patterns; F. auricularia exhibited low intrasexual genetic correlations for the dimorphic trait, suggesting that the ITC is moving towards a resolution. Meanwhile, R. echinopus exhibited high and significant intrasexual genetic correlations for most traits, suggesting that morphs in the bulb mite may be limited in evolving to their optima. This also shows that intrasexual dimorphisms can evolve despite strong genetic constraints, contrary to current predictions. We discuss the implications of this genetic constraint and emphasize the potential importance of ITC for our understanding of intrasexual dimorphisms.     

GENETIC VARIATION FOR PHENOTYPIC PLASTICITY IN THE LARVAL LIFE HISTORY OF SPADEFOOT TOADS (SCAPHIOPUS COUCHII)

Phenotypic plasticity in life-history traits is common. The relationship between phenotype and environment, or reaction norm, associated with life-history plasticity can evolve by natural selection if there is genetic variation within a population for the reaction norm and if the traits involved affect fitness. As with other traits, selection on plasticity in a particular trait or in response to a particular environmental factor may be constrained by trade-offs with other traits that affect fitness. In this paper, I experimentally evaluated broad-sense genetic variation in the reaction norms of age and size at metamorphosis in response to two environmental factors, food level and temperature. Differences among full-sib families in one or both traits were evident in all treatments. However, variation among families in their responses to each treatment (genotype-environment interaction) resulted in variation among treatments in estimated heritabilities and genetic correlations. Age at metamorphosis was equally sensitive to temperature in all families, but size at metamorphosis was more sensitive to temperature in some families than in others. Size at metamorphosis was equally sensitive to food level in all families, but age at metamorphosis was sensitive to food in some families but not in others. At high temperature or low food, the genetic correlation between age and size at metamorphosis was positive, generating a potential trade-off between metamorphosing early to attain higher larval survival and metamorphosing later to achieve larger size. This trade-off extends across treatments: families with the largest average size at metamorphosis achieved larger size with the longest average and greatest plasticity in age at metamorphosis. Other families achieved shorter average larval periods by exhibiting greater plasticity in size at metamorphosis but had the smallest average size at metamorphosis. This trade-off may reflect an underlying functional constraint on the ability to respond optimally to all environments, resulting in persistent genetic variation in reaction norms.     

ADAPTIVE GENETIC VARIATION IN GROWTH AND DEVELOPMENT OF TADPOLES OF THE HYBRIDOGENETIC RANA ESCULENTA COMPLEX

The distribution and proportion of the sexual species Rana lessonae to the hemiclonal hybrid R. esculenta among natural habitats suggests that these anurans may differ in adaptive abilities. I used a half-sib design to partition phenotypic and quantitative genetic variation in tadpole responses at two food levels into causal variance components. Rana lessonae displays strong phenotypic variation across food levels. Growth rate is strictly determined by environmental factors and includes weak maternal effects. Larval period and body size at metamorphosis both contain moderate levels of additive genetic variance. The sire x food interactions and the lack of environmental correlations indicate that adaptive phenotypic plasticity is present in both of these traits. In contrast, R. esculenta displays less phenotypic variation across food levels, especially for larval period. Variation in body size at metamorphosis is underlain by genetic variation as shown by high levels of additive genetic variance, yet growth rate and larval period are not. Significant environmental correlations between larval period at high food level and growth, larval period, and body size at low food, indicate phenotypic plasticity is absent. A positive phenotypic correlation between body size at metamorphosis and larval period for R. lessonae at both food levels suggests a trade-off between growing large and metamorphosing quickly to escape predation or pond drying. The lack of a similar correlation for R. esculenta at the high food level suggests it may be less constrained. Different levels of adaptive genetic variation among larval traits suggest that the sexual species and the hybridogenetic hemiclone differ in their abilities to cope with temporally and spatially heterogeneous environments.     

Genetic covariance structure of growth in the salamander Ambystoma macrodactylum

The size of an organism at any point during ontogeny often has fitness consequences through either direct selection on size or through selection on size-related morphological, performance, or life history traits. However, the evolutionary response to selection on size across ontogeny (a growth trajectory) may be limited by genetic correlations across ages. Here we characterize the phenotypic and genetic covariance structure of length and mass growth trajectories in a natural population of larval Ambystoma macrodactylum using function-valued quantitative genetic analyses and principal component decomposition. Most of the phenotypic and genetic variation in both growth trajectories appears to be confined to a single principal component describing a pattern of positive covariation among sizes across all ages. Higher order principal components with no significant associated genetic variation were identified for both trajectories, suggesting that evolution towards certain patterns of negative covariation between sizes across ages is constrained. The well-characterized positive relationship between size at metamorphosis and fitness in pond-breeding amphibians predicts that the across-age covariance structure will strongly limit evolution only if there is negative selection on size prior to metamorphosis. The pattern of genetic covariation observed in this study is similar to that observed in other vertebrate taxa, indicating that size may often be highly genetically and phenotypically integrated across ontogeny. Additionally, we find that phenotypic and genetic analyses of growth trajectories can yield qualitatively similar patterns of covariance structure.     

Genetic variability predicts common frog (Rana temporaria) size at metamorphosis in the wild

We investigated associations between genetic variability and two fitness-related traits--size and age at metamorphosis--in two subartic populations of the common frog, Rana temporaria. We found that metamorphic size was positively correlated with individual heterozygosity (as estimated using eight microsatellite loci) and that maternal heterozygosity also explained a significant amount of variation in this trait. In contrast, age at metamorphosis was only explained by environmental factors. Since size at metamorphosis is positively correlated with fitness in amphibians, these results suggest that genetic variability may be an important component of individual fitness in common frogs. The environmental variation underlying timing of metamorphosis may indicate that strong selection pressure on this trait in the Nordic environment is likely to override genetic effects.     

Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies

The cane toad (Rhinella marina) is one of the most successful invasive species worldwide, and has caused significant negative impacts on Australian fauna. Experimental work in the laboratory and in mesocosms has shown that tadpoles of native frogs can affect survival, size at metamorphosis and duration of larval period of cane toad tadpoles. To test if these effects occur in nature, we conducted a field experiment using two temporary ponds where we set up enclosures with tadpoles of native green tree frogs (Litoria caerulea) and cane toads in treatments with a range of densities and combinations. The presence of green tree frog tadpoles significantly decreased the growth rate of toad tadpoles and increased the duration of their larval period in both ponds; in one pond, frog tadpoles also significantly reduced the body length and mass of metamorph toads. Toad tadpoles did not have any significant negative effects on green tree frog tadpoles, but there was strong intraspecific competition within the latter species: increased frog tadpole density resulted in increased larval period and reduced survival, growth rate and size at metamorphosis for frogs at one or both ponds. Our results are encouraging for the possibility of using native frogs as one component of an integrated approach to the biological control of cane toads.     

Habitat predictors of genetic diversity for two sympatric wetland‐breeding amphibian species

Population genetic diversity is widely accepted as important to the conservation and management of wildlife. However, habitat features may differentially affect evolutionary processes that facilitate population genetic diversity among sympatric species. We measured genetic diversity for two pond‐breeding amphibian species (Dwarf salamanders, Eurycea quadridigitata; and Southern Leopard frogs, Lithobates sphenocephalus) to understand how habitat characteristics and spatial scale affect genetic diversity across a landscape. Samples were collected from wetlands on a longleaf pine reserve in Georgia. We genotyped microsatellite loci for both species to assess population structures and determine which habitat features were most closely associated with observed heterozygosity and rarefied allelic richness. Both species exhibited significant population genetic structure; however, structure in Southern Leopard frogs was driven primarily by one outlier site. Dwarf salamander allelic richness was greater at sites with less surrounding road area within 0.5 km and more wetland area within 1.0 and 2.5 km, and heterozygosity was greater at sites with more wetland area within 0.5 km. In contrast, neither measure of Southern Leopard frog genetic diversity was associated with any habitat features at any scale we evaluated. Genetic diversity in the Dwarf salamander was strongly associated with land cover variables up to 2.5 km away from breeding wetlands, and/or results suggest that minimizing roads in wetland buffers may be beneficial to the maintenance of population genetic diversity. This study suggests that patterns of genetic differentiation and genetic diversity have associations with different habitat features across different spatial scales for two syntopic pond‐breeding amphibian species.     

Apoptosis in amphibian organs during metamorphosis

During amphibian metamorphosis, the larval tissues/organs rapidly degenerate to adapt from the aquatic to the terrestrial life. At the cellular level, a large quantity of apoptosis occurs in a spatiotemporally-regulated fashion in different organs to ensure timely removal of larval organs/tissues and the development of adult ones for the survival of the individuals. Thus, amphibian metamorphosis provides us a good opportunity to understand the mechanisms regulating apoptosis. To investigate this process at the molecular level, a number of thyroid hormone (TH) response genes have been isolated from several organs of Xenopus laevis tadpoles and their expression and functional analyses are now in progress using modern molecular and genetic technologies. In this review, we will first summarize when and where apoptosis occurs in typical larva-specific and larval-to-adult remodeling amphibian organs to highlight that the timing of apoptosis is different in different tissues/organs, even though all are induced by the same circulating TH. Next, to discuss how TH spatiotemporally regulates the apoptosis, we will focus on apoptosis of the X. laevis small intestine, one of the best characterized remodeling organs. Functional studies of TH response genes using transgenic frogs and culture techniques have shown that apoptosis of larval epithelial cells can be induced by TH either cell-autonomously or indirectly through interactions with extracellular matrix (ECM) components of the underlying basal lamina. Here, we propose that multiple intra- and extracellular apoptotic pathways are coordinately controlled by TH to ensure massive but well-organized apoptosis, which is essential for the proper progression of amphibian metamorphosis.     

An invasive species imposes selection on life‐history traits of a native frog

As well as their direct ecological impacts on native taxa, invasive species can impose selection on phenotypic attributes (morphology, physiology, behaviour, etc.) of the native fauna. In anurans, body size at metamorphosis is a critical life‐history trait: for most challenges faced by post‐metamorphic anurans, larger size at metamorphosis probably enhances survival. However, our studies on Australian frogs (Limnodynastes convexiusculus) show that this pattern can be reversed by the arrival of an invasive species. When metamorph frogs first encounter invasive cane toads (Bufo marinus), they try to eat the toxic invader and, if they are able to do so, are likely to die from poisoning. Because frogs are gape‐limited predators, small metamorphs cannot ingest a toad and thus survive long enough to disperse away from the natal pond (and thus from potentially deadly toads). These data show that larger size at metamorphosis can reduce rather than increase anuran survival rates, because larger metamorphs are more easily able to ingest (and thus be poisoned by) metamorph cane toads. Our results suggest that patterns of selection on life‐history traits of native taxa (such as size and age at metamorphosis, seasonal timing of breeding and duration of pondside aggregation prior to dispersal) can be modified by the arrival of an invasive species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 329–336.     

Crosses between frog populations reveal genetic divergence in larval life history at short geographical distance

A number of studies have documented interpopulation divergence in amphibian larval life-history traits across latitudes. Because many frogs are philopatric and have a patchy habitat distribution, genetic divergence could also exist on a much smaller geographical scale, revealed by recent estimates of population divergence using molecular markers. Whether this divergence is reflected in phenotypic traits is virtually unknown. Using artificial fertilization, individuals of the common frog, Rana temporaria , were crossed from two populations situated 130 km apart and differing in population size. The pattern of size at metamorphosis showed evidence of non-additive effects, as demonstrated by a significant interaction between male and female population of origin. Outbreeding resulted in an increase in metamorph size when eggs from the small population were fertilized with sperm from the large population. In the reciprocal cross, however, the pattern was in the opposite direction, with no significant effect of male population of origin. Genetic divergence of populations separated by a relatively short geographical distance may be more common in frogs than previously acknowledged, with potential implications for conservation of declining amphibian species.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 189–195.     

Within-Population Developmental and Morphological Plasticity is Mirrored in Between-Population Differences: Linking Plasticity and Diversity

It has been suggested that phenotypic plasticity can facilitate evolutionary diversification of organisms. If life-history and morphological diversification across a lineage is mirrored in diversification in the same traits due to phenotypic plasticity within a lineage it fulfils one of the expectations that are needed to support this diversification hypothesis. We carried out a laboratory study to examine development rate and morphology between and within populations of the parsley frog, Pelodytes punctatus. We found that frogs reared in the laboratory had a longer development time, relatively longer hind legs and relatively narrower heads under constant water level compared to those under decreasing water level simulating pool drying. This adaptive phenotypic plasticity response to pool drying was mirrored across populations because frogs from permanent waters had longer development times, relatively longer hind legs and relatively narrower heads compared to frogs from temporary waters. Hence the developmental and morphological plasticity observed within populations was also observed between populations as constitutive expressed traits. We suggest that the morphology pattern observed was driven by a common developmental process (time to metamorphosis), indicating that plasticity may contribute to evolutionary change, ultimately resulting in genetic accommodation of the morphological traits.     

Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration

The evolution of environmentally-induced changes in phenotype or reaction norm implies both the existence at some time of genetic variation within a population for that plasticity measured by the presence of genotype x environment interaction (G x E), and that phenotypic variation affects fitness. Otherwise, the genetic structure of polygenic traits may restrict the evolution of the reaction norm by the lack of independent evolution of a given trait in different environments or by genetic trade-offs with other traits that affect fitness. In this paper, we analyze the existence of G x E in metamorphic traits to two environmental factors, larval density and pond duration in a factorial experiment with Bufo calamita tadpoles in semi-natural conditions and in the laboratory. Results showed no plastic temporal response in metamorphosis to pond durability at low larval density. The rank of genotypes did not change across different hydroperiods, implying a high genetic correlation that may constrain the evolution of the reaction norm. At high larval density a significant G x E interaction was found, suggesting the potential for the evolution of the reaction norm. A sibship (#1) attained the presumed “optimal” reaction norm by accelerating developmental rate in short duration ponds and delaying it in longer ponds. This could be translated in fitness by an increment in metamorphic survival and size at metamorphosis in short and long ponds respectively with respect to non-plastic sibships. However, genetic variability for plasticity suggests that optimal reaction norm for developmental rates may be variable and hard to achieve in the heterogeneous pond environment. Mass at metamorphosis was not plastic across different pond durations but decreased at high larval density. Significant adaptive plasticity for growth rates appeared in environments that differed drastically in level of crowding conditions, both in the field and in the laboratory. The fact that survival of juveniles metamorphosed at high density ponds was a monotonic function of metamorphic size, implies that response to selection may occur in this population of natterjacks and that genetic variability in plasticity may be a reliable mechanism maintaining adaptive genetic variation in growth rates in the highly variable pond environment.     

Detritus Quality and Locality Determines Survival and Mass,but Not Export,of Wood Frogs at Metamorphosis

Single-site experiments have demonstrated detritus quality in wetlands can have strongly negative, neutral, and even positive influences on wildlife. However, an examination of the influence of detritus quality across several regions is lacking and can provide information on whether impacts from variation in detritus quality are consistent across species with wide ranges. To address this gap in regional studies we examined effects of emergent and allochthonous detritus of different nutrient qualities on amphibians and assessed a mechanism that may contribute to potential impacts. We used aquatic mesocosms to raise wood frogs (Rana sylvatica) from two regions of the United States with whole plants from purple loosestrife (Lythrum salicaria), leaf litter from native hardwood trees, and a mixture of both. We examined several metrics of amphibian fitness and life history, including survival, number of days to metamorphosis, and size at metamorphosis. Further, we quantified whether the effects of detritus type could translate to variation in anuran biomass or standing stock of nitrogen or phosphorus export. Our results show detritus with high nutrient quality (purple loosestrife) negatively influenced survival of wood frogs, but increased size of metamorphic individuals in two different regions of the United States. Despite the decrease in survival, the increase in size of post-metamorphic anurans raised with high quality detritus resulted in anuran biomass and standing stock of N and P export being similar across treatments at both locations. These results further demonstrate the role of plant quality in shaping wetland ecosystem dynamics, and represent the first demonstration that effects are consistent within species across ecoregional boundaries.     

Competition among herbivores of Solanum carolinense as a constraint on the evolution of host-plant resistance

Interspecific competition (or facilitation) between herbivores sharing a host plant species can result in negative (or positive) correlations in damage levels, independent of a plant’s genetic covariance in resistance to the herbivores. Just like genetic correlations in resistance to herbivory, these “environmental correlations” in damage may affect the evolution of resistance in the host plant. In a field study of 960 ramets and 40 genets of the herbaceous plant Solanum carolinense, I looked for evidence of such environmental correlations in damage caused by 11 species of herbivores, including 10 insects and 1 mammal. There were 28 significant correlations in damage levels between species (21 negative and 7 positive) after plant genetic influences on resistance were statistically removed. Negative environmental correlations were more likely between species that fed upon the same type of plant organs than between those that fed on different types of organs, and the magnitudes of the correlations were inversely proportional to the abundance of the organ types. Taken together, these results offer strong evidence that competition is largely responsible for the pattern of environmental correlations in damage. Environmental correlations were just as common as genetic correlations in resistance, but the environmental correlations tended to be lower in magnitude, were more likely to be negative, and were more evenly spread out among the herbivore community than the genetic correlations. Damage levels by all 11 species were negatively correlated with damage by at least one other species. Thus the selective advantage a plant would receive from increased resistance any of these herbivores would be partially negated by increased damage by competing herbivores. As a result, competition has the potential to be an important constraint on the evolution of resistance in S. carolinense.