The larval habit of constructing and carrying a portable case has evolved many times in the Holometabola. It is a widespread trait of the Trichoptera and Lepidoptera (e.g. the Coleophoridae and Psychidae). Among the Coleoptera, casebearing is found in four related subfamilies of the Chrysomelidae, the so-called camptosomates: Clytrinae, Cryptocephalinae, Chlamisinae, and Lamprosomatinae (Boving and Craighead 1931). The larval case of many insects is thought to function primarily in defense by providing armor or camouflage (Otto and Svensson 1980). Here we describe the uses of the case and other defenses in a chlamisine beetle, Exema canadensis Pierce, and speculate briefly on the evolution and consequences of the case-bearing habit. The genus Exema Lacordaire contains nine species in North America (Karren 1966). All of the species appear to be univoltine and to feed on a fairly restricted range of herbaceous or shrubby genera in the Asteraceae (Jenks 1940; Karren 1966, 1972). In central New York E. canadensis is commonly found on goldenrods {Solidago spp.) and asters {Aster spp.). Its life cycle was summarized by Messina and Root (1980). Le Sage (1982) recently described the immature stages.

Polygenic genome-wide association mapping identified two regions of the cowpea genome associated with different components of resistance to its major post-harvest pest, the seed beetle Callosobruchus maculatus. Cowpea (Vigna unguiculata) is an important grain and fodder crop in arid and semi-arid regions of Africa, Asia, and South America, where the cowpea seed beetle, Callosobruchus maculatus, is a serious post-harvest pest. Development of cultivars resistant to C. maculatus population growth in storage could increase grain yield and quality and reduce reliance on insecticides. Here, we use a MAGIC (multi-parent, advanced-generation intercross) population of cowpea consisting of 305 recombinant inbred lines (RILs) to identify genetic variants associated with resistance to seed beetles. Because inferences regarding the genetic basis of resistance may depend on the source of the pest or the assay protocol, we used two divergent geographic populations of C. maculatus and two complementary assays to measure several aspects of resistance. Using polygenic genome-wide association mapping models, we found that the cowpea RILs harbor substantial additive-genetic variation for most resistance measures. Variation in several components of resistance, including larval development time and survival, was largely explained by one or several linked loci on chromosome 5. A second region on chromosome 8 explained increased seed resistance via the induction of early-exiting larvae. Neither of these regions contained genes previously associated with resistance to insects that infest grain legumes. We found some evidence of gene–gene interactions affecting resistance, but epistasis did not contribute substantially to resistance variation in this mapping population. The combination of mostly high heritabilities and a relatively consistent and simple genetic architecture increases the feasibility of breeding for enhanced resistance to C. maculatus.

Genes that affect adaptive traits have been identified, but our knowledge of the genetic basis of adaptation in a more general sense (across multiple traits) remains limited. We combined population-genomic analyses of evolve and resequence experiments, genome-wide association mapping of performance traits, and analyses of gene expression to fill this knowledge gap, and shed light on the genomics of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus. Using population-genomic approaches, we detected modest parallelism in allele frequency change across replicate lines during adaptation to lentil. Mapping populations derived from each lentil-adapted line revealed a polygenic basis for two host-specific performance traits (weight and development time), which had low to modest heritabilities. We found less evidence of parallelism in genotype-phenotype associations across these lines than in allele frequency changes during the experiments. Differential gene expression caused by differences in recent evolutionary history exceeded that caused by immediate rearing host. Together, the three genomic data sets suggest that genes affecting traits other than weight and development time are likely to be the main causes of parallel evolution, and that detoxification genes (especially cytochrome P450s and beta-glucosidase) could be especially important for colonization of lentil by C. maculatus.

AbstractEnvironmental stress can have a profound effect on inbreeding depression. Quantifying this effect is of particular importance in threatened populations, which are often simultaneously subject to both inbreeding and environmental stress. But while the prevalence of inbreeding–stress interactions is well known, the importance and broader applicability of such interactions in conservation are not clearly understood. We used seed beetles, Callosobruchus maculatus, as a model system to quantify how environmental stressors (here host quality and temperature stress) interact with inbreeding as measured by changes in the magnitude of inbreeding depression, δ, as well as the relative importance of inbreeding–stress interactions to overall fitness. We found that while both environmental stressors caused substantial inbreeding–stress interactions as measured by change in δ, the relative importance of these interactions to overall survival was modest. This suggests that assessing inbreeding–stress interactions within the framework of δ alone may give an inaccurate representation of the relevance of interactions to population persistence. Furthermore, we found that the effect of environmental stress on fitness, but not inbreeding depression, varied strongly among populations. These results suggest that the outcomes of inbreeding–stress interactions are not easily generalized, an important consideration in conservation settings.

The ability to adapt to a novel host plant may vary among insect populations with different genetic histories, and colonization of a marginal host may be facilitated by genetic admixture of disparate populations. We assembled populations of the seed beetle, Callosobruchus maculatus (F.), from four continents, and compared their ability to infest two hosts, lentil and pea. We also formed two cross-continent hybrids (Africa x N.A. and Africa x S.A.). In pre-selection assays, survival was only similar to 3% in lentil and similar to 40% in pea. For three replicate populations per line, colonization success on lentil was measured as cumulative exit holes after 75-175 d. On pea, we estimated the change in larval survival after five generations of selection. Females in all lines laid few eggs on lentil, and survival of F-1 larvae was uniformly <5%. Subsequently, however, the lines diverged considerably in population growth. Performance on lentil was highest in the Africa x N.A. hybrid, which produced far more adults (mean > 11,000) than either parental line. At the other extreme, Asian populations on lentil appeared to have gone extinct. The Africa x N.A. line also exhibited the highest survival on pea, and again performed better than either parent line. However, no line displayed a rapid increase in survival on pea, as is sometimes observed on lentil. Our results demonstrate that geographic populations can vary substantially in their responses to the same novel resource. In addition, genetic admixtures (potentially caused by long-distance transport of infested seeds) may facilitate colonization of an initially poor host.

Rapid adaptation can prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics (e.g., rates and patterns of allele frequency change) and genomic basis of successful rescue, particularly in multicellular organisms. We conducted an evolve-and-resequence experiment to investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus , when it is experimentally shifted to a stressful host plant, lentil. Low survival (∼1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population, with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. Selection on these loci was only moderately consistent in time, but parallel evolutionary changes were evident in sublines formed after the lentil line had passed through a bottleneck. By comparing estimates of selection and genomic change on lentil across five independent C. maculatus lines (the new lentil-adapted line, three long-established lines, and one case of failed evolutionary rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary changes. Overall, our results suggest that evolutionary rescue in this system can be caused by very strong selection on multiple loci driving rapid and pronounced genomic change.

Cowpea, Vigna unguiculata (L.) Walp., serves as a major source of dietary protein in many tropical and subtropical regions around the world. To identify loci associated with agronomically desirable traits, eight elite cowpea cultivars were systematically inter-crossed for eight generations to yield 305 recombinant inbred lines. Here, we investigated whether these founder parents also possess resistance to the seed beetle Callosobruchus maculatus (F.), a highly destructive post-harvest pest. We estimated larval survival in seeds, egg-to-adult development time, adult mass at emergence, and seed acceptance for oviposition. Survival varied significantly among cowpea cultivars, but the pattern was complicated by an unexpected source of mortality; on three cultivars, mature larvae in a substantial fraction of seeds (20-36%) exited seeds prematurely, and consequently failed to molt into viable adults. Even if such seeds were eliminated from the analysis, survival in the remaining seeds varied from 49 to 92% across the eight parents. Development time and body mass also differed among hosts, with particularly slow larval development on three closely related cultivars. Egg-laying females readily accepted all cultivars except one with a moderately rugose seed coat. Overall, suitability ranks of the eight cultivars depended on beetle trait; a cultivar that received the most eggs (IT82E-18) also conferred low survival. However, one cultivar (IT93K-503-1) was a relatively poor host for all traits. Given the magnitude of variation among parental cultivars, future assays of genotyped recombinant progeny can identify genomic regions and candidate genes associated with resistance to seed beetles.

Cosmopolitan pests can consist of geographic populations that differ in their current host ranges or in their ability to colonize a novel host. We compared the responses of cowpea-adapted, seed-beetle populations (Callosobruchus maculatus [F.] (Coleoptera: Chrysomelidae: Bruchinae)) from Africa, North America, and South America to four novel legumes: chickpea, lentil, mung bean, and pea. We also qualitatively compared these results to those obtained earlier for an Asian population. For each host, we measured larval survival to adult emergence and used both no-choice and choice tests to estimate host acceptance. The pattern of larval survival was similar among populations: high or moderately high survival on cowpea, mung bean, and chickpea, intermediate survival on pea, and very low survival on lentil. One exception was unusually high survival of African larvae on pea, and there was modest variation among populations for survival on lentil. The African population was also an outlier with respect to host acceptance; under no-choice conditions, African females showed a much greater propensity to accept the two least preferred hosts, chickpea and lentil. However, greater acceptance of these hosts by African females was not evident in choice tests. Inferences about population differences in host acceptance can thus strongly depend on experimental protocol. Future selection experiments can be used to determine whether the observed population differences in initial performance will affect the probability of producing self-sustaining populations on a marginal crop host.

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life-history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co-occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition-related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness-related traits of insect populations.

Colonization of new environments can lead to rapid changes in fitness-related traits. For herbivorous insects, switching to a new host plant can be comparable to invading a new habitat. Behavioral, physiological, and life-history traits commonly vary among insect populations associated with different plants, but how host shifts cause trait divergence is often unclear. We investigated whether experimental host shifts would modify a key insect trait, egg-laying behavior, in a seed beetle. Beetle populations associated long-term with either a small-seeded host (mung bean) or a large-seeded host (cowpea) were switched to each other’s host. After 36–55 generations, we assayed three aspects of oviposition behavior known to differ between the mung bean- and cowpea-adapted populations. Responses to the host shifts were asymmetrical. Females from lines transferred from mung bean to cowpea produced less uniform distributions of eggs among seeds, were more likely to add an egg to an occupied seed, and were more likely to “dump” eggs when seeds were absent. These lines thus converged toward the cowpea-adapted population. In contrast, the reciprocal host shift had no effect; oviposition behavior was unchanged in lines transferred from cowpea to mung bean. We suggest that these results reflect an asymmetry in the fitness consequences of each host shift, which in turn depended on differences in larval competitiveness in the original populations. Interactions among multiple fitness components are likely to make evolutionary responses less predictable in novel environments.

1. Adapting to a low‐quality plant may require modification of an insect's digestive physiology, oviposition behaviour, or other host‐use traits. If colonising a marginal host entails a cost, a decay in adaptation would be expected after selection is relaxed, i.e. if populations on a novel host are reverted to their high‐quality ancestral host.2. Replicate lines of the seed beetle Callosobruchus maculatus (F.) rapidly adapted to lentil seeds; larval survival rose from approximately 1 to ≥ 90%, and oviposition on lentil increased more than two‐fold. This study compared egg‐laying behaviour in lines that either remained on lentil or were reverted to the ancestral host, mung bean, for 22–62 generations.3. Consistent with the trade‐off hypothesis, females from two reverted sublines showed decreased oviposition on lentil (estimated as lifetime fecundity), but host acceptance in a third subline was unchanged. In a short‐term assay, acceptance of lentil by newly emerged females was lower in each reverted subline than in the corresponding non‐reverted one. Because effective population sizes (determined from genome resequencing) were large throughout the experiment, this decline in host acceptance is unlikely to be explained solely by genetic drift.4. Variation among replicates in the magnitude of the reversion effect was also observed in a previous study of larval survival. However, the pattern of variation for survival was not congruent with the pattern of variation for host acceptance in this study. Thus, genes mediating improved performance on lentil appear to be largely independent of those responsible for increased oviposition.

Trade-offs have often been invoked to explain the evolution of ecological specialization. Phytophagous insects have been especially well studied, but there has been little evidence that resource-based trade-offs contribute to the evolution of host specialization in this group. Here, we combine experimental evolution and partial genome resequencing of replicate seed beetle selection lines to test the trade-off hypothesis and measure the repeatability of evolution. Bayesian estimates of selection coefficients suggest that rapid adaptation to a poor host (lentil) was mediated by standing genetic variation at multiple genetic loci and involved many of the same variants in replicate lines. Sublines that were then switched back to the ancestral host (mung bean) showed a more gradual and variable (less repeatable) loss of adaptation to lentil. We were able to obtain estimates of variance effective population sizes from genome-wide differences in allele frequencies within and between lines. These estimates were relatively large, which suggests that the contribution of genetic drift to the loss of adaptation following reversion was small. Instead, we find that some alleles that were favored on lentil were selected against during reversion on mung bean, consistent with the genetic trade-off hypothesis.

Experimental evolution has provided little support for the hypothesis that the narrow diets of herbivorous insects reflect trade-offs in performance across hosts; selection lines can sometimes adapt to an inferior novel host without a decline in performance on the ancestral host. An alternative approach for detecting trade-offs would be to measure adaptation decay after selection is relaxed, that is, when populations newly adapted to a novel host are reverted to the ancestral one. Lines of the seed beetle Callosobruchus maculatus rapidly adapted to a poor host (lentil); survival in lentil seeds increased from 2% to >90% in <30 generations. After the lines had reached a plateau with respect to survival in lentil, sublines were reverted to the ancestral host, mung bean. Twelve generations of reversion had little effect on performance in lentil, but after 25-35 generations, the reverted lines exhibited lower survival, slower development and smaller size. The most divergent pair of lines was then assayed on both lentil and mung bean. Performance on lentil was again much poorer in the reverted line than in the nonreverted one, but the lines performed equally well on mung bean. Moreover, the performance of the nonreverted line on mung bean remained comparable to that of the original mung-bean population. Our results thus present a paradox: loss of adaptation to lentil following reversion implies a trade-off, but the continued strong performance of lentil-adapted lines on mung bean does not. Genomic comparisons of the reverted, nonreverted and ancestral lines may resolve this paradox and determine the importance of selection vs. drift in causing a loss of adaptation following reversion.

Adaptation to one novel host plant may simultaneously improve an insect's performance on other unfamiliar hosts, as a kind of cross‐adaptation. In selection experiments using an Asian population of the seed beetle C allosobruchus maculatus ( F abricius) ( C oleoptera: C hrysomelidae: B ruchinae), larval survival in lentil seeds increased from about 1 to >90% in fewer than 30 generations, and acceptance of lentil by egg‐laying females increased two‐ to three‐fold. We examined whether rapid adaptation to lentil altered beetle performance on other grain legumes, including hosts more closely related to lentil than to the ancestral host, mung bean. Three replicate, lentil‐adapted lines were compared to the mung‐bean (control) line with respect to both host acceptance (oviposition under no‐choice conditions) and larval performance (survival to adult emergence, development time, and adult mass at emergence). In most experiments, females from the lentil lines laid more eggs on unfamiliar hosts than did females from the mung‐bean line. Greater oviposition on novel hosts could not be explained by variation in potential fecundity, and did not appear to depend on a host's relatedness to lentil. Although survival in lentil remained extremely divergent between the mung‐bean and lentil lines (0 vs. >90%), the lines did not differ in larval performance on two other novel hosts (pea and fava bean) that are much more closely related to lentil than to mung bean. Because larval performance is most likely the limiting factor in the potential colonization of a novel host by C . maculatus , our experiments did not provide strong evidence for cross‐adaptation. The results suggest that adaptation to even a highly marginal host need not lead to a general expansion of an insect's host range.

Geographic populations of a widespread species can differ in their ability to adapt to a novel environment because they possess different amounts of the requisite genetic variation. We compared responses to the same novel host in ecologically and genetically divergent populations of the seed beetle Callosobruchus maculatus (F.). Populations from Africa and Asia had been derived from and maintained on different legume hosts. In preselection assays, both populations exhibited lower survival, slower development, and smaller size on a third host (adzuki bean), and the difference in performance between the ancestral and novel hosts was especially high for the African population. Replicate lines of each population were switched to adzuki bean or maintained on the ancestral host, and beetle performance was measured on both hosts after 12 generations. Survival on adzuki bean increased substantially in the adzuki-bean lines of the African population, but improved only slightly in the Asian lines. Similarly, only the African adzuki-bean lines exhibited significantly faster development on adzuki bean. Improved performance on adzuki bean did not simultaneously reduce performance on the ancestral host. Together with previous studies, these results confirm that populations of C. maculatus often possess sufficient standing genetic variation for rapid adaptation to a novel host, but the magnitude of the response may depend on the source population. Although international trade in grain legumes can expand beetle host ranges and produce unusual biotypes, the consistent absence of strong genetic trade-offs in larval performance or adult oviposition across hosts makes it unlikely that this insect would form distinct host races.

Inbreeding is well known to have adverse effects on fitness-related traits in insects, but less is known about its effect on behavior, particularly outside the context of mating success. We used the seed beetle Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchinae) to determine the effect of moderate inbreeding (inbreeding coefficient F = 0.25) on host discrimination, that is, the ability of ovipositing females to avoid occupied hosts and thereby reduce competition among larval offspring. Inbreeding depression was simultaneously estimated for morphological (body mass), physiological (egg hatch), and life-history (realized fecundity) traits in the same population. Compared with outbred females, inbred females exhibited an 11% reduction in mass, a 9% reduction in fecundity, and a small (4%) but significant reduction in egg hatching success. Nearly all of the decline in fecundity among inbred females could be explained by the decline in body mass. In contrast to the other three traits, host discrimination was unaffected by inbreeding. Inbred females actually distributed their eggs slightly more uniformly among seeds than did outbred females, but this difference disappeared after we corrected for inbreeding effects on fecundity. An assay of doubly inbred females (F = 0.375) confirmed that the tendency to avoid occupied hosts is immune to moderate inbreeding. The lack of inbreeding depression for host discrimination suggests that heritable variation for the trait within populations (as detected in previous studies) is largely caused by alleles with additive rather than dominant effects, and contrasts with predictions based on population crosses.

Seeds of many arid habitat plants have a water-impermeable coat and can germinate only after being scarified. Bruchine seed beetles are important parasites of legume seeds in these environments, but their effect on germination can be unpredictable. Beetles deplete seed resources and can kill the embryo but also scarify seeds. We investigated the effects of a generalist parasite, Stator limbatus, on the germination and growth of two common legumes in the Sonoran desert, catclaw acacia (Acacia greggii) and blue paloverde (Parkinsonia florida). Feeding damage from a single larva greatly increased germination of paloverde but not acacia. This benefit was reduced if seeds were attacked by multiple larvae. Beetle-damaged seeds of both hosts germinated more quickly than did control seeds. Infestation by beetles reduced seedling size, though effects were greater for paloverde than for acacia. Our results demonstrate that the effect of S. limbatus can be highly host-specific. In addition, beetle infestation may enhance or reduce seedling recruitment, depending on the availability of other scarifying agents and the number of larvae per seed. Such contingencies make it difficult to predict the net effect of seed beetles on efforts to control invasive legume hosts or establish native hosts during aridland restoration. (C) 2011 Elsevier Ltd. All rights reserved.