Do parasitoids diversify in response to host‐plant shifts by herbivorous insects?

1. For herbivorous insects, the incorporation of a novel host into the diet, and subsequent formation of distinct host associations (races), is thought to be a significant early step in the speciation process. While many studies have addressed this issue, virtually nothing is known about the evolutionary response of natural enemies to herbivore host‐race formation. 2. The hypothesis that the parasitoid wasp Eurytoma gigantea (Hymenoptera: Eurytomidae) has formed host races in direct response to the host shift and subsequent host‐race formation by its host, the gallmaker Eurosta solidaginis (Diptera: Tephritidae) was tested. Emergence time, mating preference, and female oviposition preference were determined for parasitoids derived from galls of each Eurosta host race. 3. Male and female E. gigantea overlap broadly in their emergence times from each Eurosta host race, suggesting that there is no phenological barrier to gene flow. 4. In choice experiments, female parasitoids did not mate assortatively: females that emerged from one Eurosta host race were equally likely to mate with males from either Eurosta host race. 5. Oviposition behaviour experiments revealed that female parasitoids do not prefer to oviposit on their host race of origin and that there is no overall preference for one host race, even though fitness is higher when parasitoids are reared from Eurosta galls of the Solidago gigantea host race than when reared from Eurosta galls of the Solidago altissima host race. 6. These results suggest that E. gigantea has not diverged in parallel with its host in response to the herbivore host‐plant shift. Further studies are needed before the ubiquity of this diversification mechanism can be evaluated fully.     

Evolutionary radiation of Asteromyia carbonifera (Diptera: Cecidomyiidae) gall morphotypes on the goldenrod Solidago altissima (Asteraceae)

Population divergence of phytophagous insects is often coupled to host‐plant shifts and is frequently attributed to the divergent selective environments associated with alternative host‐plants. In some cases, however, divergence is associated with the use of alternative host‐plant organs of a single host species. The basis of within‐host radiations such as these remains poorly understood. In the present stusy, we analysed the radiation of Asteromyia gall midges occurring both within one host plant species and within a single organ on that host. In this system, four morphologically distinct Asteromyia gall forms (morphs) coexist on the leaves of goldenrod Solidago altissima. Our analyses of amplified fragment length polymorphism and DNA sequence data confirm the genetic differentiation among midges from three gall morphs and reveal evidence of a genetically distinct fourth gall morph. The absence of clear gall morph related clades in the mitochondrial DNA derived phylogenies is indicative of incomplete lineage sorting or recent gene flow, suggesting that population divergence among gall forms is recent. We assess the likely history of this radiation and use the results of phylogenetic analyses along with ecological data on phenology and parasitism rates to evaluate potential hypotheses for the mode of differentiation. These preliminary analyses suggest that diversification of the Asteromyia gall morphs is likely shaped by interactions between the midge, a symbiotic fungus, and parasitoid enemies. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 840–858.     

Host‐associated divergence in sympatric host races of the leaf beetle Lochmaea capreae: implications for local adaptation and reproductive isolation

Ecological specialization is widely recognized as a major determinant of the emergence and maintenance of biodiversity. We studied two critical facets of specialization – local adaptation and habitat choice – in the host races of the leaf beetle Lochmaea capreae on willow and birch. Our results revealed that there is asymmetric disruptive selection for host use traits, and host races achieved different adaptive sets of life history traits through association with their host plant. Beetles from each host race exhibited food and oviposition preference for their own host plant. Reciprocal transplant displayed significant variation in host acceptance and performance: all families from the willow race rejected the alternative host plant before initiation of feeding and all died on this host plant. By contrast, all families from the birch race accepted willow for feeding, but they consumed less and performed less well. Intriguingly, families that performed well on birch also performed well on willow, suggesting positive genetic correlation rather than genetic trade‐offs. Our results suggest that the major proximal determinant of host specialization in the willow race is the behavioural acceptance of a plant rather than the toxicity of the food resource. However, in the birch race a combination of behavioural host acceptance and performance may play a role in specialization. Our study sheds light on the mechanisms by which divergent host adaptation might influence the evolution of reproductive isolation between herbivorous populations.     

Nutrition as a facilitator of host‐race formation: the shift of a stem‐boring beetle to a gall host

1. The importance of host‐race formation to herbivorous insect diversity depends on the likelihood that successful populations can be established on a new plant host. A previously unexplored ecological aid to success on a novel host is better nutritional quality. The role of nutrition was examined in the shift of the stem‐boring beetle Mordellistena convicta to fly‐induced galls on goldenrod and the establishment there of a genetically distinct gall host race. 2. First, larvae of the host race inhabiting stems of Solidago gigantea were transplanted into stems and galls of greenhouse‐grown S. gigantea plants. At the end of larval development, the mean mass of larvae transplanted to galls was significantly greater than the mass of larvae transplanted to stems, indicating a likely nutritional benefit during the shift. This advantage was slightly but significantly diminished when the gall‐inducing fly feeding at the centre of the gall died early in the season. Additionally, there was a suggestion of a trade‐off in the increased mortality of smaller beetle larvae transplanted into galls. 3. In a companion experiment, S. gigantea gall‐race beetle larvae were likewise transplanted to S. gigantea stems and galls. Besides the expected greater mass in galls, the larvae also exhibited adaptations to the gall nutritional environment: larger inherent size, altered tunnelling behaviour, and no diminution of mass pursuant to gall‐inducer mortality. 4. In a third line of inquiry, chemical analyses of field‐collected S. gigantea plants revealed higher levels of mineral elements important to insect nutrition in galls as compared with stems.     

The role of olfactory cues in the sequential radiation of a gall‐boring beetle,Mordellistena convicta

1. Herbivorous insects often have close associations with specific host plants, and their preferences for mating and ovipositing on a specific host‐plant species can reproductively isolate populations, facilitating ecological speciation. Volatile emissions from host plants can play a major role in assisting herbivores to locate their natal host plants and thus facilitate assortative mating and host‐specific oviposition. 2. The present study investigated the role of host‐plant volatiles in host fidelity and oviposition preference of the gall‐boring, inquiline beetle, Mordellistena convicta LeConte (Coleoptera: Mordellidae), using Y‐tube olfactometers. Previous studies suggest that the gall‐boring beetle is undergoing sequential host‐associated divergence by utilising the resources that are created by the diverging populations of the gall fly, Eurosta solidaginis Fitch (Diptera: Tephritidae), which induces galls on the stems of goldenrods including Solidago altissima L. (Asteraceae) and Solidago gigantea Ait. 3. Our results show that M. convicta adults are attracted to galls on their natal host plant, avoid the alternate host galls, and do not respond to volatile emissions from their host‐plant stems. 4. These findings suggest that the gall‐boring beetles can orient to the volatile chemicals from host galls, and that beetles can use them to identify suitable sites for mating and/or oviposition. Host‐associated mating and oviposition likely play a role in the sequential radiation of the gall‐boring beetle.     

Trade‐off between fecundity and survival generates stabilizing selection on gall size

Complex interactions within multitrophic communities are fundamental to the evolution of individual species that reside within them. One common outcome of species interactions are fitness trade‐offs, where traits adaptive in some circumstances are maladaptive in others. Here, we identify a fitness trade‐off between fecundity and survival in the cynipid wasp Callirhytis quercusbatatoides that induces multichambered galls on the stem of its host plant Quercus virginiana. We first quantified this trade‐off in natural populations by documenting two relationships: a positive association between the trait gall size and fecundity, as larger galls contain more offspring, and a negative association between gall size and survival, as larger galls are attacked by birds at a higher rate. Next, we performed a field‐based experimental evolution study where birds were excluded from the entire canopy of 11 large host trees for five years. As a result of the five‐year release from avian predators, we observed a significant shift to larger galls per tree. Overall, our study demonstrates how two opposing forces of selection can generate stabilizing selection on a critical phenotypic trait in wild populations, and how traits can evolve rapidly in the predicted direction when conditions change.     

The role of ecological availability and host plant characteristics in determining host use by the bogus yucca moth Prodoxus decipiens

1. Specialisation in host plant use is strongly correlated with speciation in many plant‐feeding insects. Specialised taxa, however, could be restricted in host range due to limits in ecological availability of host plant species rather than trade‐offs in using alternate host species. 2. Moths in the genus Prodoxus are extreme specialists on Yucca and speciation is closely tied to host plant shifts. However, many Yucca ranges are allopatric. This study examined whether the bogus yucca moth Prodoxus decipiens is limited in host range because of biogeographic factors or due to differences in the characteristics of host plant species. 3. In a common garden, local P. decipiens moths that use Yucca filamentosa were exposed to individuals of five Yucca species, two that are known hosts of P. decipiens in other parts of its range and three that are used by its sister species, Prodoxus quinquepunctellus. 4. Local moths were attracted to flowers of all Yucca species and females attempted oviposition in the flowering stalks of all species. However, larvae successfully completed development to diapause in only one of the five host plant species. Larval development on non‐natal Yucca species was significantly reduced compared with the local host. 5. The results suggest that differences in host plant characteristics among Yucca species would result in strong natural selection during a host shift. Thus, specialisation in host plant use is probably due to trade‐offs involved with using novel host plant species as well as ecological availability.     

The evolution of novel host use is unlikely to be constrained by trade‐offs or a lack of genetic variation

The genetic and ecological factors that shape the evolution of animal diets remain poorly understood. For herbivorous insects, the expectation has been that trade‐offs exist, such that adaptation to one host plant reduces performance on other potential hosts. We investigated the genetic architecture of alternative host use by rearing individual Lycaeides melissa butterflies from two wild populations in a crossed design on two hosts (one native and one introduced) and analysing the genetic basis of differences in performance using genomic approaches. Survival during the experiment was highest when butterfly larvae were reared on their natal host plant, consistent with local adaptation. However, cross‐host correlations in performance among families (within populations) were not different from zero. We found that L. melissa populations possess genetic variation for larval performance and variation in performance had a polygenic basis. We documented very few genetic variants with trade‐offs that would inherently constrain diet breadth by preventing the optimization of performance across hosts. Instead, most genetic variants that affected performance on one host had little to no effect on the other host. In total, these results suggest that genetic trade‐offs are not the primary cause of dietary specialization in L. melissa butterflies.     

The effects of becoming taller: direct and pleiotropic effects of artificial selection on plant height in Brassica rapa

Plant height is an important trait for plant reproductive success. Plant height is often under pollinator‐mediated selection, and has been shown to be correlated with various other traits. However, few studies have examined the evolutionary trajectory of plant height under selection and the pleiotropic effects of plant height evolution. We conducted a bi‐directional artificial selection experiment on plant height with fast cycling Brassica rapa plants to estimate its heritability and genetic correlations, and to reveal evolutionary responses to artificial selection on height and various correlated traits. With the divergent lines obtained through artificial selection, we subsequently conducted pollinator‐choice assays and investigated resource limitation of fruit production. We found that plant height variation is strongly genetically controlled (with a realized heritability of 41–59%). Thus, plant height can evolve rapidly under phenotypic selection. In addition, we found remarkable pleiotropic effects in phenology, morphology, floral scent, color, nectar and leaf glucosinolates. Most traits were increased in tall‐line plants, but flower size, UV reflection and glucosinolates were decreased, indicating potential trade‐offs. Pollinators preferred plants of the tall selection lines over the short selection lines in both greenhouse experiments with bumblebees and field experiment with natural pollinators. We did not detect any differences in resource limitation between plants of the different selection lines. Overall, our study predicts that increased height should evolve under positive pollinator‐mediated directional selection with potential trade‐offs in floral signals and herbivore defense.     

Carnivores and carotenoids are associated with adaptive behavioural divergence in a radiation of gall midges

1. Adaptive divergence in sympatry is supposed to be inhibited by the homogenizing role of gene flow. However, studies continue to uncover examples of sympatric divergence. In this study, two divergent phenotypes in a complex of four syntopic gall midge morphotypes [nominally Asteromyia carbonifera Osten Saken, Diptera: Cecidomyiidae: Alycaulini] are characterised. The first is a behavioural phenotype governing within‐host tissue preference and the second is a trait governing accessory‐gland carotenoid quality and quantity. 2. One gall morphotype (crescents) lay most of their eggs on mature tissue whereas the other three gall morphotypes oviposit only on young emerging leaves. Ecological maintenance of this divergent trait appears to be driven by enemy‐reduced space. That is, nearly 40% of the crescent morphotype galls that develop high on the plant are attacked by the egg parasitoid Platygaster solidaginis Ashmed, whereas those low on the plant are relatively protected. 3. All morphotypes contain carotenoids in their accessory glands, but the quality and quantity of these pigments differs significantly between the morphotypes and is positively associated with the probability of parasitism by P. solidaginis. 4. Larval salivary glands also contain carotenoids and the plant hormone abscisic acid, which in plants is synthesized from carotenoid precursors and is involved in regulating plant defences. This hormone may facilitate gall development and influence gall morphology. 5. Ecological fitness trade‐offs between carotenoids, parasitoid attack, and plant resistance may be fostering adaptive divergence in ovipositional phenotypes and sympatric speciation in this complex of gall midge morphotypes.     

THE JACK OF ALL TRADES IS MASTER OF NONE: A PATHOGEN'S ABILITY TO INFECT A GREATER NUMBER OF HOST GENOTYPES COMES AT A COST OF DELAYED REPRODUCTION

A trade‐off between a pathogen's ability to infect many hosts and its reproductive capacity on each host genotype is predicted to limit the evolution of an expanded host range, yet few empirical results provide evidence for the magnitude of such trade‐offs. Here, we test the hypothesis for a trade‐off between the number of host genotypes that a fungal pathogen can infect (host genotype range) and its reproductive capacity on susceptible plant hosts. We used strains of the oat crown rust fungus that carried widely varying numbers of virulence (avr) alleles known to determine host genotype range. We quantified total spore production and the expression of four pathogen life‐history stages: infection efficiency, time until reproduction, pustule size, and spore production per pustule. In support of the trade‐off hypothesis, we found that virulence level, the number of avr alleles per pathogen strain, was correlated with significant delays in the onset of reproduction and with smaller pustule sizes. Modeling from our results, we conclude that trade‐offs have the capacity to constrain the evolution of host genotype range in local populations. In contrast, long‐term trends in virulence level suggest that the continued deployment of resistant host lines over wide regions of the United States has generated selection for increased host genotype range.     

Comparative genome scan detects host‐related divergent selection in the grasshopper Hesperotettix viridis

In this study, we used a comparative genome scan to examine patterns of population differentiation with respect to host plant use in Hesperotettix viridis, a Nearctic oligophagous grasshopper locally specialized on various Asteraceae including Solidago, Gutierrezia, and Ericameria. We identified amplified fragment length polymorphism (AFLP) loci with significantly elevated F_ST (outlier loci) in multiple different‐host and same‐host comparisons of populations while controlling for geographic distance. By comparing the number and identities of outlier loci in different‐host vs. same‐host comparisons, we found evidence of host plant‐related divergent selection for some population comparisons (Solidago‐ vs. Gutierrezia‐feeders), while other comparisons (Ericameria‐ vs. Gutierrezia‐feeders) failed to demonstrate a strong role for host association in population differentiation. In comparisons of Solidago‐ vs. Gutierrezia‐feeding populations, a relatively high number of outlier loci observed repeatedly in different‐host comparisons (35% of all outliers and 2.7% of all 625 AFLP loci) indicated a significant role for host‐related selection in contributing to overall genomic differentiation in this grasshopper. Mitochondrial DNA sequence data revealed a star‐shaped phylogeny with no host‐ or geography‐related structure, low nucleotide diversity, and high haplotype diversity, suggesting a recent population expansion. mtDNA data do not suggest a long period of isolation in separate glacial refugia but are instead more compatible with a single glacial refugium and more recent divergence in host use. Our study adds to research documenting heterogeneity in differentiation across the genome as a consequence of divergent natural selection, a phenomenon that may occur as part of the process of ecological speciation.     

STRONG SELECTION GENOME‐WIDE ENHANCES FITNESS TRADE‐OFFS ACROSS ENVIRONMENTS AND EPISODES OF SELECTION

Fitness trade‐offs across episodes of selection and environments influence life‐history evolution and adaptive population divergence. Documenting these trade‐offs remains challenging as selection can vary in magnitude and direction through time and space. Here, we evaluate fitness trade‐offs at the levels of the whole organism and the quantitative trait locus (QTL) in a multiyear field study of Boechera stricta (Brassicaceae), a genetically tractable mustard native to the Rocky Mountains. Reciprocal local adaptation was pronounced for viability, but not for reproductive components of fitness. Instead, local genomes had a fecundity advantage only in the high latitude garden. By estimating realized selection coefficients from individual‐level data on viability and reproductive success and permuting the data to infer significance, we examined the genetic basis of fitness trade‐offs. This analytical approach (Conditional Neutrality‐Antagonistic Pleiotropy, CNAP) identified genetic trade‐offs at a flowering phenology QTL (costs of adaptation) and revealed genetic trade‐offs across fitness components (costs of reproduction). These patterns would not have emerged from traditional ANOVA‐based QTL mapping. Our analytical framework can be applied to other systems to investigate fitness trade‐offs. This task is becoming increasingly important as climate change may alter fitness landscapes, potentially disrupting fitness trade‐offs that took many generations to evolve.     

Variable selection on Eurosta's gall size,III: Can an evolutionary response to selection be detected?

Standard quantitative genetic theory predicts that when a trait is exposed to selection, the between-generation change in the phenotypic mean, Δz?_i, will be equal to the product of the trait's heritability and the selection differential, h²S. By extension, this theory implies that if a number of replicate populations are exposed to varying intensities of selection, the between-generation changes in means should covary with the selection differential applied. This relationship offers an opportunity for a statistical test to detect evolutionary change when selection is measured in replicate populations. If an evolutionary response to phenotypic selection occurs, the regression of over S_i, where i indicates population, will have a positive slope. This statistical test was applied to data on the insect Eurosta solidaginis (Diptera: Tephritidae). The larvae of this fly induce galls on the stems of the host plant, Solidago altissima (Asteraceae). Previous work has shown that gall size is a heritable trait of the insect. Further, size-dependent attack on Eurosta larvae by parasitoids selects for larger gall size (Weis and Abrahamson, 1986). Long-term data on phenotypic selection in 16 populations across 5 generations were analyzed for selection response. Apparent upward evolutionary responses were seen in 2 of the 4 between-generation transitions. However, no response was seen when the analysis was applied to the cumulative change in gall size. Examination of the data suggested that some of the change in mean gall size was a developmental response to spatial and temporal variation in the environment. Non-linear developmental effects of environment, when combined with non-linear fitness functions, can induce a spurious selection response; these non-linear relationships can account for the apparent evolutionary change gall size found in the by-generation analysis. Thus, there is no reliable evidence for evolutionary change in Eurosta's gall size over the generations studied. Stasis of gall size in the face of ongoing selection may be due to counterbalancing selection on the gallmaker imposed by host plant resistance.     

Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies

Summary Larvae of the tephritid fly Eurosta solidaginis induce ball-shaped galls on the stem of tall goldenrod, Solidago altissima. Survival probability depends on gall size; in small galls the larva is vulnerable to parasitoid oviposition, whereas larvae in large galls are more frequently eaten by avian predators. Fly populations from 20 natural old fields in central Pennsylvania were monitored in 1983 and 1984 to examine the distribution of the selection intensity imposed by natural enemies, the parasitoids Eurytoma gigantea and E. obtusiventris, the inquiline Mordellistena unicolor, and the predatory birds Dendrocopus pubescens and Parus atricapillus. Mordellistena and E. obtusiventris are able to attack galls of all diameters while E. gigantea and the predatory birds preferentially assaulted small and large diameter galls, respectively. Eurosta in intermediate sized galls had the highest survivorship, hence selection had a stabilizing component. However, parasitoid attack was more frequent than bird attack, and the two did not exactly balance, thus there was also a directional component. The mean directional selection intensity on gall size was 0.21 standard deviations of the mean, indicating that larger gall size was favored. Interactions among the insect members of the Eurosta natural enemy guild are complex and frequent.     

Local adaptation and ecological genetics of host-plant specialization in a leaf beetle

The tendency of insect species to evolve specialization to one or a few plant species is probably a major reason for the remarkable diversity of herbivorous insects. The suggested explanations for this general trend toward specialization include a range of evolutionary mechanisms, whose relative importance is debated. Here we address two potentially important mechanisms: (i) how variation in the geographic distribution of host use may lead to the evolution of local adaptation and specialization; (ii) how selection for specialization may lead to the evolution of trade‐offs in performance between different hosts. We performed a quantitative genetic experiment of larval performance in three different populations of the alpine leaf beetle Oreina elongata reared on two of its main host plants. Due to differences in host availability, each population represents a distinctly different selective regime in terms of host use including selection for specialization on one or the other host as well as selection for utilizing both hosts during the larval stage. The results suggest that selection for specialization has lead to some degree of local adaptations in host use: both single‐host population had higher larval growth rate on their respective native host plant genus, while there was no difference between plant treatments in the two‐host population. However, differences between host plant treatments within populations were generally small and the degree of local adaptation in performance traits seems to be relatively limited. Genetic correlations in performance traits between the hosts ranged from zero in the two‐host population to significantly positive in the single‐host populations. This suggests that selection for specialization in single host populations typically also increased performance on the alternative host that is not naturally encountered. Moreover, the lack of a positive genetic correlation in the two host‐population give support for the hypothesis that performance trade‐offs between two host plants may typically evolve when a population have adapted to both these plants. We conclude that although there is selection for specialization in larval performance traits it seems as if the genetic architecture of these traits have limited the divergence between populations in relative performance on the two hosts.     

Antiherbivore defenses alter natural selection on plant reproductive traits

While many studies demonstrate that herbivores alter selection on plant reproductive traits, little is known about whether antiherbivore defenses affect selection on these traits. We hypothesized that antiherbivore defenses could alter selection on reproductive traits by altering trait expression through allocation trade‐offs, or by altering interactions with mutualists and/or antagonists. To test our hypothesis, we used white clover, Trifolium repens, which has a Mendelian polymorphism for the production of hydrogen cyanide—a potent antiherbivore defense. We conducted a common garden experiment with 185 clonal families of T. repens that included cyanogenic and acyanogenic genotypes. We quantified resistance to herbivores, and selection on six floral traits and phenology via male and female fitness. Cyanogenesis reduced herbivory but did not alter the expression of reproductive traits through allocation trade‐offs. However, the presence of cyanogenic defenses altered natural selection on petal morphology and the number of flowers within inflorescences via female fitness. Herbivory influenced selection on flowers and phenology via female fitness independently of cyanogenesis. Our results demonstrate that both herbivory and antiherbivore defenses alter natural selection on plant reproductive traits. We discuss the significance of these results for understanding how antiherbivore defenses interact with herbivores and pollinators to shape floral evolution.     

Phylogenetic analysis reveals positive correlations between adaptations to diverse hosts in a group of pathogen‐like herbivores

A jack of all trades can be master of none—this intuitive idea underlies most theoretical models of host‐use evolution in plant‐feeding insects, yet empirical support for trade‐offs in performance on distinct host plants is weak. Trade‐offs may influence the long‐term evolution of host use while being difficult to detect in extant populations, but host‐use evolution may also be driven by adaptations for generalism. Here we used host‐use data from insect collection records to parameterize a phylogenetic model of host‐use evolution in armored scale insects, a large family of plant‐feeding insects with a simple, pathogen‐like life history. We found that a model incorporating positive correlations between evolutionary changes in host performance best fit the observed patterns of diaspidid presence and absence on nearly all focal host taxa, suggesting that adaptations to particular hosts also enhance performance on other hosts. In contrast to the widely invoked trade‐off model, we advocate a “toolbox” model of host‐use evolution in which armored scale insects accumulate a set of independent genetic tools, each of which is under selection for a single function but may be useful on multiple hosts.     

Relaxation of herbivore‐mediated selection drives the evolution of genetic covariances between plant competitive and defense traits

Insect herbivores are important mediators of selection on traits that impact plant defense against herbivory and competitive ability. Although recent experiments demonstrate a central role for herbivory in driving rapid evolution of defense and competition‐mediating traits, whether and how herbivory shapes heritable variation in these traits remains poorly understood. Here, we evaluate the structure and evolutionary stability of the G matrix for plant metabolites that are involved in defense and allelopathy in the tall goldenrod, Solidago altissima. We show that G has evolutionarily diverged between experimentally replicated populations that evolved in the presence versus the absence of ambient herbivory, providing direct evidence for the evolution of G by natural selection. Specifically, evolution in an herbivore‐free habitat altered the orientation of G , revealing a negative genetic covariation between defense‐ and competition‐related metabolites that is typically masked in herbivore‐exposed populations. Our results may be explained by predictions of classical quantitative genetic theory, as well as the theory of acquisition‐allocation trade‐offs. The study provides compelling evidence that herbivory drives the evolution of plant genetic architecture.     

Effects of pathogen exposure on life‐history variation in the gypsy moth (Lymantria dispar)

Investment in host defences against pathogens may lead to trade‐offs with host fecundity. When such trade‐offs arise from genetic correlations, rates of phenotypic change by natural selection may be affected. However, genetic correlations between host survival and fecundity are rarely quantified. To understand trade‐offs between immune responses to baculovirus exposure and fecundity in the gypsy moth (Lymantria dispar), we estimated genetic correlations between survival probability and traits related to fecundity, such as pupal weight. In addition, we tested whether different virus isolates have different effects on male and female pupal weight. To estimate genetic correlations, we exposed individuals of known relatedness to a single baculovirus isolate. To then evaluate the effect of virus isolate on pupal weight, we exposed a single gypsy moth strain to 16 baculovirus isolates. We found a negative genetic correlation between survival and pupal weight. In addition, virus exposure caused late‐pupating females to be identical in weight to males, whereas unexposed females were 2–3 times as large as unexposed males. Finally, we found that female pupal weight is a quadratic function of host mortality across virus isolates, which is likely due to trade‐offs and compensatory growth processes acting at high and low mortality levels, respectively. Overall, our results suggest that fecundity costs may strongly affect the response to selection for disease resistance. In nature, baculoviruses contribute to the regulation of gypsy moth outbreaks, as pathogens often do in forest‐defoliating insects. We therefore argue that trade‐offs between host life‐history traits may help explain outbreak dynamics.