Frank J. Messina

Plant Protection as a Consequence of an Ant‐Membracid Mutualism: Interactions on Goldenrod (Solidago Sp.)

In central New York, two chrysomelid beetles, Trirhabda virgata and T. borealis, frequently cause severe defoliation of tall goldenrod, Solidago altissima. This plant is also the primary host of Publilia concava (Membracidae), a sap—feeding treehopper that is tended by ants, especially Formica spp. Staged encounters indicate that Formica ants attack adult Trirhabda beetles on goldenrod stems bearing membracids. Such stems escape defoliation by Trirhabda, and show greater mean height increment and seed production than their nearest neighbors without ants. The degree of plant protection depends on the duration of Formica presence. During Trirhabda outbreaks, only stems bearing Formica ants for most of the season are likely to produce flowers and seeds. While Formica ants do not exclude Trirhabda larvae from goldenrod stems, they do deter feeding; plants with Formica ants experience significantly less defoliation by larvae than neighboring stems without ants. Two smaller, less aggressive an species (Prenolepis imparis and Myrmica sp.) do not affect either larval or adult beetle densities.

Life-History Variation in a Seed Beetle: Adult Egg-Laying vs. Larval Competitive Ability

SummaryPopulations of the seed beetle Callosobruchus maculatus differ genetically in several traits that mediate intraspecific competition. This study examined competitive interactions between larvae from two strains that differed in their propensity to oviposit on occupied hosts. In a strain (S) where females avoided laying >1 egg/seed, larvae were highly competitive; if two larvae entered a small host simultaneously, only one adult emerged. In a strain (I) whose females were “sloppier” in their egg-laying decisions, more than half of the seeds bearing two larvae yielded two adults. If seeds contained one larva from each strain, only one adult emerged per seed, and 70% of these adults belonged to the more competitive S strain. A larvas probability of emergence could be increased if it entered the seed before its competitor. A two-day headstart was needed merely for I larvae to compete equally with S larvae. Competition also affected development time and adult weight, but its effect was highly strain- and sex-specific. Adult life-history traits also differed substantially between strains. Compared to I beetles, S beetles exhibited decreased longevity, lower fecundity, a truncated period of oviposition, and larger egg and body size. Fecundity was linearly related to body size in the I strain, but was largely independent of size in the S strain. When faced with a shortage of hosts, S females (whose progeny are highly competitive) “withheld” eggs and died without depositing 40% of their lifetime supply. In contrast, the fecundity of I females was independent of seed availability. Comparisons with previous studies suggest that both highly uniform egg-laying and strong interference among larvae may be a consequence of chronic association with a relatively small host. Results from the larval competition experiments were used as parameter estimates for a simple, game-theoretic model that postulates interference vs. exploitative strategies. Fitness comparisons suggest that a strategy employing interference competition cannot be invaded by a more exploitative form of competition in a small host.

Environment‐dependent reversal of a life history trade‐off in the seed beetle Callosobruchus maculatus

Abstract 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.

Ability of ovipositing seed beetles to discriminate between seeds with differing egg loads

Abstract. 1. Previous work has shown that ovipositing females of Callosobruchus maculatus (F.) avoid seeds already bearing eggs, and thereby reduce competition among their larval progeny within seeds.

Heritability and ‘evolvability’ of fitness components in Callosobruchus maculatus

Heritabilities of traits closely related to fitness (e.g. life-history traits) tend to be lower than those of morphological traits in natural populations. It is unclear, however, whether this pattern reflects relatively low additive-genetic variation, relatively high residual variation (i.e. non-additive and environmental effects) or both. A standard, half-sib breeding design was used to estimate narrow-sense heritabilities and coefficients of additive-genetic variation (CVA) for a life-history trait (total fecundity), a morphological trait (wing length) and a behavioural trait (allocation of eggs among available resources) in two outbred populations of the seed beetle Callosobruchus maculatus. Heritabilities of fecundity and wing length were high in both populations whereas the heritability of egg-laying behaviour was low but non-zero. In contrast, estimates of ‘evolvability’, which depend on CVA, were highest for fecundity, intermediate for egg-laying behaviour and lowest for wing length. These results resemble those from a recent survey of Drosophila studies and suggest that the typically low heritabilities of behavioural or life-history traits are better explained by high residual variation than by low additive-genetic variation. Phenotypic and genetic correlations were generally not significant except for a positive relationship between wing length and fecundity. No evidence was obtained of a trade-off or underlying functional relationship between the number of eggs laid and the pattern of egg dispersion among available resources.

PREDICTABLE MODIFICATION OF BODY SIZE AND COMPETITIVE ABILITY FOLLOWING A HOST SHIFT BY A SEED BEETLE

Abstract 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 ≤65% if larvae were from the cowpea lines but ≥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.

Intraspecific variation in the egg-spacing behavior of the seed beetleCallosobruchus maculatus

Females of Callosobruchus maculatustend to distribute their eggs uniformly among host seeds and, thereby, reduce competition among larvae within seeds. We investigated variability in this behavior by assaying beetles from seven geographic strains on each of three host species. To quantify egg-spacing behavior,we devised an index (U)that estimates the uniformity of the egg distribution but is independent of the number of eggs laid. Egg-spacing behavior was highly variable among beetle strains and legume hosts. Females from an Indian strain frequently achieved the most uniform distribution possible (maximum hyperdispersion), whereas females from two Brazilian strains frequently deposited eggs randomly. Differences among strains were evident throughout the period of oviposition;some strains were “sloppy” when even egg densities were low. Variation in egg-spacing behavior appears to be influenced by prior host associations and by host size. The most well-developed spacing behavior was observed in a strain associated with the smallest host, which supports only one or two larvae per seed. Realized fecundity also varied significantly among beetle strains. We found no evidence, however, of a predicted tradeoff between the number of eggs laid and the uniformity of the egg dispersion.

Expression of a Life-History Trade-Off in a Seed Beetle Depends on Environmental Context

Within populations of the seed beetle Callosobruchus maculatus (F.) (Coleoptera: Bruchidae), female longevity is positively correlated with fecundity, both phenotypically and genetically. Yet manipulations of egg‐laying rate (through deprivation of seeds or mates) consistently suggest a trade‐off between these traits. In this study, females were exposed to four levels of seed availability and the relationship between fecundity and longevity was examined both across and within environments. The expected trade‐off was observed across environments, as females with few or no seeds laid fewer eggs and lived longer than females with many seeds. Within environments, however, the relationship was inconsistent; individual longevity and fecundity were positively correlated when seeds were abundant, uncorrelated when seeds were few and negatively correlated when seeds were absent. Body mass at adult emergence was positively correlated with fecundity, but its effect was stronger when seeds were present than when they were absent. After the effects of mass were statistically controlled, longevity and fecundity remained positively correlated among females with many seeds and negatively correlated among those without seeds. Thus, even a single technique (phenotypic correlation) can produce divergent conclusions about the ‘cost of reproduction’ in insects. The reversal in the correlation appears to depend on variation in reproductive allocation; when seeds are scarce or absent, differences in reproductive effort among individuals may be large enough to overwhelm differences in resource acquisition.

Plant Architecture and the Foraging Success of Ladybird Beetles Attacking the Russian Wheat Aphid

We examined the interaction between the fourteen‐spotted ladybird beetle, Propylea quatuordecimpunctata (L.), and the Russian wheat aphid, Diuraphis noxia (Mordvilko), on two grasses with divergent leaf architectures. Like wheat, crested wheatgrass bears flat, broad leaves, whereas Indian ricegrass produces slender, tightly rolled leaves. In the absence of aphid prey, residence times and time budgets of larvae and adults of P. quatuordecimpunctata were similar on the two hosts, although larvae tended to remain longer on crested wheatgrass. When aphids were present, both predator stages dislodged, contacted, and captured aphids at higher rates on Indian ricegrass than on crested wheatgrass. Predator time budgets and behavior sequences also reflected a greater predation risk for D. noxia on Indian ricegrass, and were consistent with earlier, population‐level experiments in the field. Comparisons between aphid‐free and aphid‐infested plants suggest that the effect of host plant in this tri‐trophic system largely depended on differences in the availability of prey refuges rather than on differences in predator searching behavior; proportionally more aphids fed in exposed locations on Indian ricegrass than on crested wheatgrass. Plant architecture is likely to be an important component of the predation risk of D. noxia because of the aphids tendency to feed in relatively concealed locations.

Genetic architecture of population differences in oviposition behaviour of the seed beetle Callosobruchus maculatus

Few studies have examined the genetic architecture of population differences in behaviour and its implications for population differentiation and adaptation. Even fewer have examined whether differences in genetic architecture depend on the environment in which organisms are reared or tested. We examined the genetic basis of differences in oviposition preference and egg dispersion between Asian (SI) and African (BF) populations of the seed beetle, Callosobruchus maculatus. We reared and tested females on each of two host legumes (cowpea and mung bean). The two populations differed in mean oviposition preference (BF females preferred cowpea seeds more strongly than did SI females) and egg dispersion (SI females distributed eggs more uniformly among seeds than did BF females). Observations of hybrid and backcross individuals indicated that only the population difference in oviposition preference could be explained by complete additivity, whereas substantial dominance and epistasis contributed to the differences in egg dispersion. Both rearing host and test host affected the relative magnitude of population differences in egg dispersion and the composite genetic effects. Our results thus demonstrate that the relative influence of epistasis and dominance on the behaviour of hybrids depends on the behaviour measured and that different aspects of insect oviposition are under different genetic control. In addition, the observed effect of rearing host and oviposition host on the relative importance of dominance and epistasis indicates that the genetic basis of population differences depends on the environment in which genes are expressed.