Proximate effects of maternal oviposition preferences on defense efficacy and larval survival in a diet-specialized tortoise beetle. Who knows best: mothers or their progeny?

Authors: VENCL, FREDERIC - Smithsonian Tropical Research; PLATA, CAMILA - University Of Los Andes; Srygley, Robert

Submitted to: Ecological Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2013
Publication Date: 9/18/2013
Citation: Vencl, F.V., Plata, C.A., Srygley, R.B. 2013. Proximate effects of maternal oviposition preferences on defense efficacy and larval survival in a diet-specialized tortoise beetle. Who knows best: mothers or their progeny? Ecological Entomology. 38(6):596-607.

Interpretive Summary: Insects that feed on plants might lay their offspring on leaves that maximize growth, but females might also choose sites that minimize risk of predation. Investigating a beetle with maternally guarded broods that erect a fecal shield to ward off predators, we tested whether the mother’s choice of oviposition site was in the best interest of offspring survival to predatory attacks. Females preferred to lay eggs on young leaves near ground level where the larvae were more likely to be encountered by ants, and older leaves high above the ground where larvae were more likely to be encountered by wasps or bugs. Larval shields made from ingesting young leaves were a better deterrent to ants and wasps than those made from old leaves, whereas shields from old leaves were rich in phytol, a bug attractant. Maternal guarding aided larval defense from bugs and wasps in high sites, but larvae improved their chances of survival by migrating to younger leaves that were less rich in the bug attractant. Maternal selection of leaf height and age to oviposit may be at odds with the progeny’s best interest, but migration of the offspring to feed on both young and old leaves reduced vulnerability to specific predators. Thus within a single plant, site selection by the mother changes the ability of larval defenses to effectively target specific predators. Plant compounds that are precursors to bug attractants could be engineered to increase the efficacy of insect predators in crop pest control, and those that deterred ants and wasps might prove useful in the development of control agents for ants and wasps that are agricultural pests.

Technical Abstract: The 'mother-knows-best' hypothesis predicts that the fate of a larval herbivorous insect depends on its mother's ability to locate a host that fosters optimal growth. However, larval performance is often decoupled from female preference, which suggests that factors other than nutrition, such as leaf quality, host architecture, or predation, also influence fitness. We tested the hypothesis that female oviposition choices impact defense efficacy and survival in the diet-specialized leaf beetle Acromis sparsa, whose vulnerable ectophytic larvae are maternally-guarded, gregarious, and possess chemically-enhanced shields. Defense manipulations revealed that both oviposition site and leaf age impacted defense performance and larval survival. Whereas larvae near to the ground were more likely to succumb to ants, those feeding in high sites were most vulnerable to wasps and bugs. Defensive traits performed differentially against specific enemies: shields were effective in low but not in high sites. Guarding was effective against ants and bugs in high, but not in low sites. Predator impact was contingent upon leaf age. Shields derived from young leaves increased survival against ants and wasps. When they oviposited in concealed, lower sites, where ants are the major threat, mothers knew best by selecting young leaves rich in fatty acids, which become shield deterrents. In high sites on mature leaves, larvae knew best and migrated to younger leaves that contained less phytol, a compound known to attract bugs. Within-host enemy-free space may explain contrasting maternal choices (mature leaves+high sites versus young leaves+low sites) as responses to conflicting selection by different predators. Thus, site and leaf selection may be at odds with the best interests of progeny, while migration may mitigate within-host trade-offs between defense performance and vulnerability to specific predators. Guarding and migration may be behavioral adaptations critical to the exploitation of enemy-free space as well as fostering the evolution of dietary specialization.