Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore

Summary Plant resistance to insect herbivores may derive from traits influencing herbivore preference, traits influencing the suitability of the plant as a host, or both. However, the plant traits influencing host-plant selection by ovipositing insect herbivores may not completely overlap those traits that affect larval survival, and distinct traits may exhibit different levels of genetic vs. environmental control. Therefore, resource supply to the host plant could affect oviposition preference and larval performance differently in different plant genotypes. To test this hypothesis, the effects of resistance level, plant genotype, and resource supply to the host plant on oviposition preference and larval performance of a gallmaking herbivore, and on various plant traits that could influence these, were examined. Replicates of four genotypes of Solidago altissima, grown under low, medium, or high levels of nutrient supply in full sun or with medium levels of nutrients in shade, were exposed to mass-released Eurosta solidaginis. The number of plants ovipunctured was significantly affected by plant genotype and the interaction between genotype and nutrient supply to the host plant: one susceptible and one resistant genotype were more preferred, and preference tended to increase with nutrient supply in the more-preferred genotypes. The growth rate of ovipunctured plants during the oviposition period was significantly greater than that of unpunctured plants. Bud diameter (which was strongly correlated with plant growth rate), leaf area, and leaf water content were significant determinants of the percentage of plants ovipunctured, explaining 74% of the variance. The number of surviving larvae was significantly affected by plant genotype, but no effect of nutrient or light supply to the host plant was detected. The ratio of bud diameter to bud length was positively related to the percentage of ovipunctured plants that formed galls, suggesting that the accurate placement of eggs near the apical meristem by ovipositing females may be easier in short, thick buds. No significant correlation was observed between oviposition preference and larval survival at the population level. These results suggest that the plant traits affecting oviposition preference may exhibit different magnitudes of phenotypic plasticity than those affecting larval survival, and that the degree of phenotypic plasticity in plant traits affecting oviposition preference may differ among genotypes within a species.     

A quantitative genetic analysis of leaf beetle larval performance on two natural hosts: including a mixed diet

Published quantitative genetic studies of larval performance on different host plants have always compared performance on one host species or genotype vs. performance on another species or genotype. The fact that some insects may feed on more than one plant species during their development has been neglected. We executed a quantitative genetic analysis of performance with larvae of the leaf beetle Oreinaelongata, raised on each of two sympatric host plants or on a mixture of them. Growth rate was higher for larvae feeding on Adenostylesalliariae, intermediate on the mixed diet and lowest on Cirsium spinosissimum. Development time was shortest on A. alliariae, intermediate on mixed diet and longest on C. spinosissimum. Survival was higher on the mixed diet than on both pure hosts. Genetic variation was present for all three performance traits but a genotype by host interaction was found only for growth rate. However, the reaction norms for growth rate are unlikely to evolve towards an optimal shape because of a lack of heritability of growth rate in each single environment. We found no negative genetic correlations for performance traits among hosts. Therefore, our results do not support a hypothesis predicting the existence of between‐host trade‐offs in performance when both hosts are sympatric with an insect population. We conclude that the evolution of host specialized genotypes is unlikely in the study population.     

Environmental and genetic control of insect abundance and herbivory along a forest elevational gradient

Environmental conditions and plant genotype may influence insect herbivory along elevational gradients. Plant damage would decrease with elevation as temperature declines to suboptimal levels for insects. However, host plants at higher elevations may exhibit traits that either reduce or enhance leaf quality to insects, with uncertain net effects on herbivory. We examined folivory, insect abundance and leaf traits along six replicated elevational ranges in Nothofagus pumilio forests of the northern Patagonian Andes, Argentina. We also conducted a reciprocal transplant experiment between low- and high-elevation sites to test the extent of environmental and plant genetic control on insect abundance and folivory. We found that insect abundance, leaf size and specific leaf area decreased, whereas foliar phosphorous content increased, from low-, through mid- to high-elevation sites. Path analysis indicated that changes in both insect abundance and leaf traits were important in reducing folivory with increasing elevation and decreasing mean temperature. At both planting sites, plants from a low-elevation origin experienced higher damage and supported greater insect loads than plants from a high-elevation origin. The differences in leaf damage between sites were twofold larger than those between plant origins, suggesting that local environment was more important than host genotype in explaining folivory patterns. Different folivore guilds exhibited qualitatively similar responses to elevation. Our results suggest an increase in insect folivory on high-elevation N. pumilio forests under future climate warming scenarios. However, in the short-term, folivory increases might be smaller than expected from insect abundance only because at high elevations herbivores would encounter more resistant tree genotypes.     

Niche construction through germination cueing: life-history responses to timing of germination in Arabidopsis thaliana

Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.     

Distinguishing intrapopulational categories of plants by their insect faunas: galls on rabbitbrush

Within a population of rubber rabbitbrush, Chrysothamnus nauseosus, the subspecies C. nauseosus consimilis and C. nauseosus hololeucus, and a third unidentified group were better segregated by their insect galls, than by differences in plant morphology. This level of segregation was further increased when morphological measurements and counts of insect galls were analyzed simultaneously. We interpret this result to mean that plant morphology and insect distributions reflect two different, perhaps overlapping, portions of the host's genome. By using both sets of characters concurrently, rather than either set independently, we increased the portion of the plant's genome being sampled and increased the probability of detecting differences among host genotypes. Hence, knowledge of the distributions of insect galls may be useful for augmenting the level of separation, obtained by morphological measurements, among intrapopulational categories of plant genotypes. This application may be of greatest benefit when hybridization blurs morphological distinctions among plant taxa, when morphological traits are highly variable within genotypes, or when ephemeral morphological traits (e.g., leaves, flowers) are not available for measurements.     

Host‐associated differentiation in a highly polyphagous,sexually reproducing insect herbivore

Insect herbivores may undergo genetic divergence on their host plants through host‐associated differentiation (HAD). Much of what we know about HAD involves insect species with narrow host ranges (i.e., specialists) that spend part or all their life cycle inside their hosts, and/or reproduce asexually (e.g., parthenogenetic insects), all of which are thought to facilitate HAD. However, sexually reproducing polyphagous insects can also exhibit HAD. Few sexually reproducing insects have been tested for HAD, and when they have insects from only a handful of potential host‐plant populations have been tested, making it difficult to predict how common HAD is when one considers the entire species' host range. This question is particularly relevant when considering insect pests, as host‐associated populations may differ in traits relevant to their control. Here, we tested for HAD in a cotton (Gossypium hirsutum) pest, the cotton fleahopper (CFH) (Pseudatomoscelis seriatus), a sexually reproducing, highly polyphagous hemipteran insect. A previous study detected one incidence of HAD among three of its host plants. We used Amplified fragment length polymorphism (AFLP) markers to assess HAD in CFH collected from an expanded array of 13 host‐plant species belonging to seven families. Overall, four genetically distinct populations were found. One genetically distinct genotype was exclusively associated with one of the host‐plant species while the other three were observed across more than one host‐plant species. The relatively low degree of HAD in CFH compared to the pea aphid, another hemipteran insect, stresses the likely importance of sexual recombination as a factor increasing the likelihood of HAD.     

Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.     

Plant genotype affects the quality of oilseed rape (Brassica napus) for adults and larvae of the pollen beetle (Meligethes aeneus)

Plant quality is one of the main factors influencing the fitness of phytophagous insects. Plant quality can vary not only among genotypes of the same host plant species, but also relative to the insect sex or its life stage. In the present study, the performance of larvae and adults of the pollen beetle (Meligethes aeneus F., Coleoptera: Nitidulidae), a major insect pest of oilseed rape crops, is compared on six genotypes of oilseed rape (Brassica napus). All of the traits that are measured vary among genotypes, and comprise larval developmental duration, life span of unfed emerging adults and survival time of field‐sampled adults fed with pollen from the different genotypes. No correlation is found between insect performance and quantity of food available, showing that the quality of the food (i.e. pollen) is the fitness determinant for this insect species. Additionally, the performance of larvae and adults is also not correlated despite use of the same plant genotypes, suggesting that the determinants of pollen quality differ at least partially between both life stages. It is hypothesized that this may be a result of extensive differences in diet breadth between the life stages: larvae are specialists of brassicaceous plants, whereas adults are generalists. Finally, it is suggested that the manipulation of plant quality to increase pollen beetle development time may comprise a valuable strategy for favouring biological control by natural enemies of this pest; for example, as a result of extending the vulnerability window of larvae to attack by parasitoids.     

Study of genetic variation in sesame (<Emphasis Type="Italic">Sesamum indicum</Emphasis> L.) using agro-morphological traits and <Emphasis Type="Italic">ISSR</Emphasis> markers

This research was conducted to study the genetic variation among eighteen genotypes of sesame (Sesamum indicum L.) collected from various agro-climatic regions of Iran along with six exotic genotypes from the Asian countries using both agro-morphological and ISSR marker traits. The results showed significant differences among genotypes for all agro-morphological traits and a relatively high genetic coefficient of variation observed for number of fruiting branches per plant, capsules per plant, plant height and seed yield per plant. Cluster analysis based on these traits grouped the genotypes into five separate clusters. Larger interthan intra cluster distances implies the presence of higher genetic variability between the genotypes of different groups. Genotypes of two clusters with a good amount of genetic divergence and desirable agronomic traits were detected as promising genotypes for hybridization programs. The 13 ISSR primers chosen for molecular analysis revealed 170 bands, of which 130 (76.47%) were polymorphic. The generated dendrogram based on ISSR profiles divided the genotypes into seven groups. A principal coordinate analysis confirmed the results of clustering. The agro-morphological traits and ISSR markers reflected different aspects of genetic variation among the genotypes as revealed by a non significant cophenetic correlation in the Mantel test. Therefore the complementary application of both types of information is recommended to maximize the efficiency of sesame breeding programs. The discordance among diversity patterns and geographical distribution of genotypes found in this investigation implies that the parental lines for hybridization should be selected based on genetic diversity rather than the geographical distribution.     

QUANTITATIVE GENETICS OF SIZE AND PHENOLOGY OF LIFE-HISTORY TRAITS IN CHAMAECRISTA FASCICULATA

Despite numerous adaptive scenarios concerning the evolution of plant life-history phenologies few studies have examined the heritable basis for and genetic correlations among these phenologies. Documentation of genetic variation for and covariation among reproductive phenologies is important because it is this variation/covariation that will determine the potential for response to evolutionary forces. To address this problem, I conducted a breeding experiment to determine narrow-sense heritabilities for and genetic correlations among the phenologies of life-history events and plant size in Chamaecristafasciculata, a temperate summer annual plant species. Paternal families showed no evidence of heritable variation for two estimates of plant size, six measures of reproductive phenology or two fitness components. Similarly, paternal estimates of genetic correlations among these traits were low or zero. In contrast, maternal estimates of heritability suggested the influence of maternal parent on one estimate of plant size and four phenological traits. Likewise, maternal effects influenced maternal estimates of genetic correlations. These maternal effects can arise from three sources: endosperm nuclear, cytoplasmic genetic and/or maternal phenotypic. The degree to which the phenology of one life-history trait acts as a constraint on the evolution of other phenological traits depends on the source of the maternal influence in this species.     

Natal insect experience with Arabidopsis thaliana plant genotypes influences plasticity in oviposition behavior

Previous studies have shown that insect experience with secondary chemicals present in different plant species can induce behavioral changes in female oviposition preferences. However, there is a lack of information on whether insect experience with intraspecific plant variation may influence oviposition behavior. The prediction that experience with plant genotypes would affect the oviposition behavior of two crucifer insect pests was tested using a wild ecotype of Arabidopsis thaliana (L.) Heynh. (Brassicaceae) (Col‐0) and two of its genetically modified lines (35S:ESP and tgg1 tgg2), which differ in their glucosinolate hydrolysis profiles. Choice oviposition assays were performed using both naïve and experienced females of the specialist Plutella xylostella (L.) (Lepidoptera: Plutellidae) and the generalist Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae). In addition to oviposition preferences, the effect of plant genetic lines was assessed on insect traits related to development, growth, survival, and fecundity. Experience with different natal treatments (i.e., artificial diet and plant genotypes) led to changes in oviposition behavior of the diamondback moth P. xylostella; however, this effect was dependent on the specific genetic lines included in dual‐choice oviposition assays. In addition, for both moth species, experience led to female oviposition choices that would have maximized fitness of their offspring. In summary, this article suggests that insect experience with plant genotypes varying in their secondary metabolites can influence subsequent oviposition behavior. This outcome may have implications for plant‐insect coevolution and integrated pest management.     

SEX RATIO VARIATION IN A PARASITIC WASP II. DIALLEL CROSS

Sex ratio has been studied from many theoretical and empirical perspectives, but a general assumption in sex ratio research is that changes in sex ratio occur because of selection on sex ratio itself. I carried out a quantitative genetic experiment—a diallel cross among three strains—on a parasitic wasp, Muscidifurax raptor (Hymenoptera: Pteromalidae), to measure genetic variation for sex ratio. I also tested whether sex ratio may change as a consequence of selection on other life-history traits by estimating genetic covariances between sex ratio, fecundity, longevity, and development time. Most of the variation among strains could be accounted for by a maternal effect, likely caused by a microsporidian parasite that was transmitted through the West Germany (WG) strain. Genetic variation was small by comparison, but almost all traits were affected by dominance. The only significant additive genetic effect was for fecundity early in life. Upon crossing, all traits displayed heterosis: more female-biased sex ratio, greater fecundity, longer life, and faster development time. All life-history traits were correlated phenotypically, but the correlations were mainly the result of decreased performance in crosses with the WG strain that carried the microsporidian parasite. Dominance genetic correlations were also found between sex ratio, fecundity, and longevity. How the correlation between sex ratio and other life-history traits would affect sex ratio evolution depends upon the frequencies of sex-ratio genotypes within a population as well as the signs of the correlations, because sex ratio is under frequency-dependent selection whereas other traits are generally under directional selection. Although the results from crosses among laboratory populations should be approached with caution, the inbreeding depression (the difference between inbred and outcrossed progeny) found in M. raptor implies that the evolution of a female-biased sex ratio could be affected by selection for inbreeding avoidance.     

Aphid and host‐plant genotype × genotype interactions under elevated CO2

1. Elevated CO₂ can alter plant physiology and morphology, and these changes are expected to impact diet quality for insect herbivores. While the plastic responses of insect herbivores have been well studied, less is known about the propensity of insects to adapt to such changes. Genetic variation in insect responses to elevated CO₂ and genetic interactions between insects and their host plants may exist and provide the necessary raw material for adaptation. 2. We used clonal lines of Rhopalosiphum padi (L.) aphids to examine genotype‐specific responses to elevated CO₂. We used the host plant Schedonorus arundinaceus (tall fescue; Schreb), which is capable of asexual reproduction, to investigate host plant genotype‐specific effects and possible host plant‐by‐insect genotype interactions. The abundance and density of three R. padi genotypes on three tall fescue genotypes under three concentrations of CO₂ (ambient, 700, and 1000 ppm) in a controlled greenhouse environment were examined. 3. Aphid abundance decreased in the 700 ppm CO₂ concentration, but increased in the 1000 ppm concentration relative to ambient. The effect of CO₂ on aphid density was dependent on host plant genotype; the density of aphids in high CO₂ decreased for two plant genotypes but was unchanged in one. No interaction between aphid genotype and elevated CO₂ was found, nor did we find significant genotype‐by‐genotype interactions. 4. This study suggests that the density of R. padi aphids feeding on tall fescue may decrease under elevated CO₂ for some plant genotypes. The likely impact of genotype‐specific responses on future changes in the genetic structure of plant and insect populations is discussed.     

Heritability,covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment

This study explored genetic variation and co‐variation in multiple functional plant traits. Our goal was to characterize selection, heritabilities and genetic correlations among different types of traits to gain insight into the evolutionary ecology of plant populations and their interactions with insect herbivores. In a field experiment, we detected significant heritable variation for each of 24 traits of Oenothera biennis and extensive genetic covariance among traits. Traits with diverse functions formed several distinct groups that exhibited positive genetic covariation with each other. Genetic variation in life‐history traits and secondary chemistry together explained a large proportion of variation in herbivory (r² = 0.73). At the same time, selection acted on lifetime biomass, life‐history traits and two secondary compounds of O. biennis, explaining over 95% of the variation in relative fitness among genotypes. The combination of genetic covariances and directional selection acting on multiple traits suggests that adaptive evolution of particular traits is constrained, and that correlated evolution of groups of traits will occur, which is expected to drive the evolution of increased herbivore susceptibility. As a whole, our study indicates that an examination of genetic variation and covariation among many different types of traits can provide greater insight into the evolutionary ecology of plant populations and plant–herbivore interactions.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

Differential invasion success among biotypes: case of Bemisia tabaci

Studies on success or failures of biological invasions by different insect biotypes are scarce and could provide interesting insights into the traits that determine greater or lower ability to invade. Life history traits of invasive whiteflies Bemisia tabaci of the B biotype (known as a worldwide invasive biotype) and of the indigenous biotype Ms (not known as an invader anywhere in the world), both from the island of La Réunion (Indian Ocean), were compared for this purpose. In our study we demonstrated that within a cultivated host plant (tomato), the B biotype differs from the Ms by a combination of several life-history traits. This combination gives the invasive biotype an advantage over the resident both in terms of rapid demographic growth (increased intrinsic rate of increase and associated traits such as short developmental times and high fecundity) and in terms of competition (large adult and offspring sizes), without any recorded trade off. However, in the field the resident biotype remains dominant on non-cultivated hosts (weeds) and in a particular climate (high humidity). This suggests that invasive biotypes are characterized by physiological, morphological and biological adaptations to a disturbed environment created by anthropic activities at different places in the world, while resident biotypes may persist in less altered habitats.     

High genetic diversity and low structure in an endemic long-lived tree,Yucca capensis (Asparagaceae)

• Endemic species distributed in fragmented habitats are highly vulnerable to extinction because they may have low genetic diversity. However, some life-history traits can mitigate the effect of genetic drift on populations. We analysed the level and distribution of genetic variation and ancestral population size of Yucca capensis, a long-lived endemic plant of the Baja California Peninsula, Mexico. Its populations are scattered across a habitat that is suffering accelerated transformation.
• We used six nuclear microsatellites to genotype 224 individuals from 17 locations across the entire species' geographic range. We estimated polymorphisms, heterozygosity and genetic structure. We also evaluated the ancestral and recent effective size and time since the population started to change.
• We found high heterozygosity, high polymorphism and low differentiation among locations, suggesting a panmictic population across the range. We also detected a large ancestral effective population size, which suffered a strong reduction in the Mid-Holocene.
• Despite changes in environmental conditions caused by habitat modification, the high diversity and low differentiation in Y. capensis may result from its large ancestral effective size and life-history traits, such as plant longevity, clonal growth and mating system, which reduce the rate of loss of genetic variation. However, the dependence on a specialist pollinator that displays short flight range can reduce gene flow among the plant populations and could, shortly, lead them into an extinction vortex.

     

Evolution of insect-plant relationships: chemical constraints, coadaptation, and concordance of insect/plant traits

Co-adaptations, co-evolution, and co-speciation between herbivores and their host plants have been topics of interest for several decades. Difficulties in deciphering these relationships as well as physiological, biochemical, and ecological adaptations of herbivorous insects themselves are discussed here in relation to biotic and abiotic environmental factors that create temporal as well as spatial mosaics of genetic variation. Hybridization was shown in swallowtail butterflies (Papilio) (Lepidoptera: Papilionidae) to produce some trait concordance, but mostly independent geographic trait clines (physiological, biochemical, and morphological). Strong and extensive genetic introgression of Liriodendron tulipifera detoxification abilities was documented northward across the hybrid zone, presumably as a result of regional climate warming only during the last 3–4 years. These and other genetic novelties produced by hybridization may be important in speciation processes, and they also emphasize the difficulties identifying appropriate taxonomic classifications for discussing any species concept. Host plant detoxification abilities (as `key innovations') are shown capable of rapid movement between different polyphagous herbivore species independently of the host plant availability and well beyond the insect species geographical range distribution. Part of the difficulty associated with ecologically categorizing herbivore species and identifying affiliated adaptations for host plant use may be related to independent movement of various `species-diagnostic' traits. Climate-driven local selection regimes could help generate the dynamic variation observed for co-adapted, co-evolved, or non-adapted genotypes, and may produce the confusing and changing patterns of geographic mosaics seen within and among closely related herbivores. Experimental analyses of several factors that could explain the asymmetrical shapes of trait clines across the hybrid zone for tiger swallowtail butterflies are discussed.     

Genomic evidence of genetic variation with pleiotropic effects on caterpillar fitness and plant traits in a model legume

Plant–insect interactions are ubiquitous, and have been studied intensely because of their relevance to damage and pollination in agricultural plants, and to the ecology and evolution of biodiversity. Variation within species can affect the outcome of these interactions. Specific genes and chemicals that mediate these interactions have been identified, but genome‐ or metabolome‐scale studies might be necessary to better understand the ecological and evolutionary consequences of intraspecific variation for plant–insect interactions. Here, we present such a study. Specifically, we assess the consequences of genome‐wide genetic variation in the model plant Medicago truncatula for Lycaeides melissa caterpillar growth and survival (larval performance). Using a rearing experiment and a whole‐genome SNP data set (>5 million SNPs), we found that polygenic variation in M. truncatula explains 9%–41% of the observed variation in caterpillar growth and survival. Genetic correlations among caterpillar performance and other plant traits, including structural defences and some anonymous chemical features, suggest that multiple M. truncatula alleles have pleiotropic effects on plant traits and caterpillar performance (or that substantial linkage disequilibrium exists among distinct loci affecting subsets of these traits). A moderate proportion of the genetic effect of M. truncatula alleles on L. melissa performance can be explained by the effect of these alleles on the plant traits we measured, especially leaf toughness. Taken together, our results show that intraspecific genetic variation in M. truncatula has a substantial effect on the successful development of L. melissa caterpillars (i.e., on a plant–insect interaction), and further point toward traits potentially mediating this genetic effect.