Frank J. Messina

Successful host shifts by herbivorous insects may require the modification of multiple larval and adult traits. The seed beetle Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) rarely attacks lentil (Lens culinaris Medikus), which is distantly related to its typical hosts. In a previous study, larval survival in lentil seeds increased from 85% in fewer than 20 generations of laboratory selection. However, lentil is also a poor oviposition host; lifetime fecundity on lentil was initially less than a third of that on the ancestral host [ mung bean, Vigna radiata (L.) R. Wilczek ] and one fourth of females did not even recognize lentil as a potential host. This study examined the genetic lability of host acceptance. We performed both quasi-natural selection, in which replicate lines switched to lentil were compared with those remaining on mung bean, and artificial selection, in which lines were established using females from the base population that exhibited especially low or high acceptance of lentil during a short-term assay. After only five to eight generations of quasi-natural selection, lifetime fecundity on lentil was 2 to 3 times higher in the lentil lines than in the mung bean lines. Lentil-line females also accepted the novel host sooner after adult emergence. Similarly, a single generation of artificial selection was sufficient to increase oviposition on lentil in the acceptance line. Host acceptance was not genetically correlated with larval survival, which remained <2% in lines artificially selected for either high or low acceptance of lentil seeds. Although modification of oviposition behavior in this study was not nearly as striking as the increase in larval survival reported previously, the C. maculatus population possessed enough standing genetic variation in both larval physiology and adult behavior to permit rapid adaptation to a very poor host.

If host seeds are absent, females of the seed beetle Callosobruchus maculatus sometimes ‘dump’ eggs on unsuitable substrates, which causes complete larval mortality and decreases female lifespan. To understand the possible function of this behaviour, the present study examines genetic variation in dumping behaviour between and within populations. When deprived of hosts, females from an African population are much more prone to dump eggs than Asian females, most of which dump no eggs over their lifetimes. Egg dumping therefore cannot be explained as a simple, species‐wide constraint imposed by the accumulation of mature oocytes. A transfer experiment tested the hypothesis that dumping eggs improves a female’s ability to exploit the subsequent availability of seeds, perhaps by preventing a disruption of oocyte maturation. Contrary to prediction, the number of eggs laid after females are transferred to seeds is inversely related to the number dumped during deprivation. Two bidirectional selection experiments revealed heritable variation in egg‐dumping behaviour within the African population. Deprived females from the dumper line dump more than twice as many eggs as do females from the nondumper line. Pre‐adult development time is significantly longer in the nondumper line, which suggests that trade‐offs with other fitness components could maintain variation in egg‐laying behaviour within populations. The divergent responses to host availability by African and Asian females may represent a pleiotropic effect of similarly divergent responses to host quality.

Interfertile populations of the seed beetle Callosobruchus maculatus differ genetically in several behavioral, morphological, and life-history traits, including traits that affect the intensity of larval competition within seeds. Previous studies have suggested that this variation depends on differences in host size. I performed a selection experiment in which replicate beetle lines were either maintained on a small, ancestral host (mung bean) or switched to a larger, novel host (cowpea). After 40 generations, I estimated survival, development time, and adult mass on each host, both in the presence and absence of larval competition. The shift to cowpea substantially reduced body size; irrespective of rearing host, adults from the cowpea lines were more than 10% lighter than those from the mung bean lines. Switching to cowpea also improved survival and reduced development time on this host, but without decreasing performance on the ancestral host. The most striking effect of the shift to a larger host was a reduction in larval competitiveness. When two even-aged larvae co-existed within a seed, the probability that both survived to adult emergence was > or = 65% if larvae were from the cowpea lines but < or = 12% if they were from the mung bean lines. The adverse effects of competition on development time and adult mass were also less severe in the cowpea lines than in the mung bean lines. By rapidly evolving smaller size and reduced competitiveness, the cowpea lines converged toward populations chronically associated with cowpea. These results suggest that evolutionary trajectories can be predictable, and that host-specific selection can play a major role in the diversification of insect life histories. Because host shifts by small, endophagous insects are comparable to the colonization of new habitats, adaptive responses may often include traits (such as larval competitiveness) that are not directly related to host use.

Abstract.  1. Previous studies have produced conflicting results with respect to the genetic lability of host preference in the seed beetle Callosobruchus maculatus . 2. In this study, replicate lines of an Asian population were kept on an ancestral host (mung bean) or switched to a novel host (cowpea). After 40+ generations, lines were assayed for host preference (in choice tests) and host acceptance (under no‐choice conditions), and were compared to African lines chronically associated with cowpea. 3. Host preference diverged in the expected direction. When presented a mixture of cowpeas and mung beans, females from the cowpea lines laid a greater fraction of their eggs on cowpea than did females from the mung bean lines. Preference for cowpea was nearly as strong in the cowpea lines as it was in the cowpea‐adapted African lines. 4. In contrast, the experimental host shift did not affect long‐term host acceptance. African females laid more eggs if given cowpeas than if given mung beans, but realised fecundities in the cowpea and mung bean lines were similar on the two hosts. Females from all lines laid more eggs if they were reared on cowpea than on mung bean, but rearing host had no effect on either relative host acceptance or host preference. 5. Comparisons with earlier studies suggest that the lability of host preference varies among beetle populations, which precludes generalisation at the species level. Because lines were maintained under no‐choice conditions, modification of host preference probably occurred via a lower acceptance threshold for the novel host, without a concomitant change in the long‐term acceptance of the ancestral host.

Several resistant lines of wheat, Triticum aestivum (L.) (Poaceae), have been developed to control populations of the Russian wheat aphid, Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae). We examined the potential effects of D. noxia resistant lines on another aphid, the bird cherry-oat aphid (Rhopalosiphum padi (L.) (Hemiptera: Aphididae)), which commonly co-occurs with D. noxia. Because one type of resistance (mediated by the Dn1 gene) is purported to be induced rather than constitutive, we also determined the degree to which the suitability of resistant and susceptible plants is modified by previous infestation. Although resistant lines were derived from five different sources, we did not detect any differences in the population growth of R. padi on resistant and near-isogenic susceptible plants. The performance of D. noxia was reduced as expected on resistant plants but was unaffected by whether or not plants had been previously infested. In contrast, the performance of R. padi was reduced on plants that had been previously infested but was unaffected by whether plants were resistant or susceptible to D. noxia. Because neither species' performance was especially low on previously infested, resistant plants, there was no evidence that prior aphid feeding induces a higher level of resistance.

Environmental manipulations have consistently demonstrated a cost of reproduction in the capital-breeding seed beetle, Callosobruchus maculatus, as females deprived of seeds or mates lay fewer eggs and thereby increase their longevity. Yet fecundity and longevity tend to be positively correlated within populations, perhaps as a consequence of individual differences in resource acquisition. We conducted a split-brood experiment that combined a manipulation of seed availability (seeds present or absent) with a quantitative-genetic analysis of fecundity and lifespan in each environment. Each trait was significantly heritable in each environment. Seed availability not only altered mean fecundity and longevity between environments, but also modified how the traits were correlated within environments. The signs of both the phenotypic and genetic correlations switched from positive when seeds were present to negative when seeds were absent. This reversal persisted even after the effect of body mass (a potential indicator of resource acquisition) was statistically controlled. Cross-environment genetic correlations were positive but significantly less than one for each trait. We suggest that the reversal of the fecundity–longevity relationship depends on a shift in the relative importance of resource-acquisition and resource-allocation loci between environments. In particular, a cost of reproduction may be apparent at the individual level only when seeds are scarce or absent because differences in reproductive effort become large enough to overwhelm differences in resource acquisition. Despite their common dependence on resources acquired during larval stages, fecundity and lifespan in C. maculatus do not appear to be tightly coupled in a physiological or genetic sense.

We examined the effects of prior infestation by the Russian wheat aphid [Diuraphis noxia (Mordvilko)] and the bird cherry‐oat aphid [Rhopalosiphum padi (L.)] on the subsequent feeding preferences and performance of each species. Aphid colonies fed and reproduced on wheat seedlings for five days and were then removed. After a period of plant recovery, we estimated aphid population growth and feeding preferences on control and previously infested plants. Previous infestation by D. noxia had no effect on the subsequent population growth of either aphid species. Previous infestation by R. padi reduced its own subsequent growth by 50%, but had little effect on the population growth of D. noxia. When presented leaves from control plants and D. noxia‐infested plants, D. noxia adults preferred to feed on leaves from control plants; R. padi adults showed no preference. Both aphids preferred leaves from control plants to those from R. padi‐infested plants. In free‐flight cages, alates of R. padi settled more often and produced more progeny on control plants than on plants previously infested by R. padi, but their rates of settling and reproduction were unaffected by prior D. noxia infestation. Together, our results suggest specificity in both the plant response to the two aphid species (plant quality for R. padi was lowered by prior R. padi infestation but not by D. noxia infestation) and in each aphid's response to the same modification of the host plant (infestation by R. padi reduced plant quality for itself but not for D. noxia). Effects of prior infestation on the feeding preferences of R. padi were correlated with effects on performance.

We used ecotypic variation in big sagebrush (Artemisia tridentata) to examine potential trade-offs between inherent growth rate and tolerance or resistance to herbivory. Seeds were obtained from seven geographic populations, and 1,120 seedlings were established in a common garden. In one set of plots, plants were subjected to five treatments: control, regular insecticide spray, moderate browsing, severe browsing, or moderate browsing plus insecticide. Plants in a second set of plots were all untreated, and were used to estimate ambient growth, flower production, and susceptibility to herbivorous insects. In the first growing season, population differences in relative growth rate produced approximately seven-fold variation in mean biomass. Two populations of basin big sagebrush (A. tridentata tridentata) and one population of mountain big sagebrush (A. tridentata vaseyana) grew fastest; those of Wyoming big sagebrush (A. tridentata wyomingensis) showed the slowest growth. Bi-weekly application of insecticide for two growing seasons had no effect on the growth of either browsed or unbrowsed plants. All populations showed compensatory growth (but not overcompensation) in response to browsing, but the degree of compensation was unrelated to inherent growth rate. Similarly, there was no consistent relationship between plant growth rate and flower production in the second growing season. Some insects colonized fast-growing populations more frequently than slow-growing ones, but patterns of insect colonization were species-specific. At the level of geographic populations and subspecies, we found little evidence of a built-in trade-off between inherent growth rate and the ability to tolerate or resist herbivory. Because population ranks for growth rate changed substantially between seasons, attempts to correlate growth and defense characters need to account for differences in the growth trajectories of perennial plants.