Mediation of host-plant use by a glucoside in Callosobruchus maculatus F. (Coleoptera: Bruchidae)

Abstract

Callosobruchus maculatus is a bruchid beetle that develops in the seeds of 14 species of Leguminosae, but the cowpea Vigna unguiculata is its main host plant. The conditions of adaptation for a C. maculatus population originating from West Africa on a new host plant, Vicia faba, were analysed in this study. When the C. maculatus females oviposited on the seeds of V. faba, 2.4% of the larvae penetrated the cotyledons and completed their post-embryonic development. The other larvae died as soon as they began to consume the cotyledons. The presence of a glucoside, vicine, in the seeds of V. faba was the main mortality factor. Vicine is hydrolysed by intestinal β-glucosidase to a toxic aglycone, divicine, which has adverse effects on larval metabolism. From a pair of C. maculatus that developed in V. faba seeds having a high vicine content, a strain with high larval performance on these seeds was selected. The larvae of this strain could develop in pastilles of cowpea flour containing 0.1–1% vicine. A higher concentration (1.5%) caused significant mortality. Crosses between beetles of the selected and non-selected strains demonstrated that the ability to develop in the V. faba seeds had a genetic basis, and a major autosomal gene was implicated. Larvae completing their post-embryonic development in V. faba seeds were recessive homozygous for this character. The inability to develop in these seeds was due to the presence of a major dominant gene. Biochemical studies showed that midgut β-glucosidase activity was lower in the selected strain than in the non-selected strain. The ability to develop in seeds with high vicine content is probably due to partial inhibition of a gene coding for a β-glucosidase that hydrolyses vicine to the toxic form, aglycone. Vicine is transferred from the midgut to the haemolymph without chemical transformation. This adaptation to a new host plant, due to low enzymatic activity preventing the transformation of a glucoside to its toxic aglycone has a low energetic cost.