Inheritance of traits mediating a major host shift by a seed beetle, callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae)

Abstract

The genetic basis by which insects adapt to novel host plants is poorly understood, in part because genetic changes that accompany host-range expansions often cannot be distinguished from those that occurred well after the shift. We examined the inheritance of traits mediating rapid adaptation to a poor host by the seed beetle Callosobruchus maculatus (F.) (Coleoptera: Chrysomelidae: Bruchinae). For an Asian beetle population, larval survival in lentil, Lens culinaris Medikus, was initially ≈â‰̂1%, but three separate mass-selection experiments produced lines with >80% survival in <20 generations. Each lentil-adapted line (L1-3) was then crossed with the ancestral line (M) from which it had been recently derived. Survival in the parental lines was extremely divergent: >90% in all L lines versus 0% in the M line. Survival of reciprocal F1 and F2 progeny suggested additive (intermediate) inheritance, with a small dominance deviation toward the M-line parent (in the L1 cross) or the L-line parent (in the L2 and L3 crosses), and no evidence of sex-linkage or cytoplasmic effects. Progeny from backcrosses to the M line survived at a much lower rate than would be expected by additive inheritance, but the survival of L1-backcrossed progeny was consistent with simple additivity. A potential explanation for this asymmetry is that larvae deriving 75% of their genes from the M line only rarely reach a threshold of enzymatic activity needed to detoxify lentil seeds. Two other fitness components, egg-to-adult developmental time and adult mass, also were intermediate in hybrids, but quantitative comparisons were precluded by a lack of M-line adults emerging from lentil. Additive expression of initially rare alleles can account for rapid colonization of a marginal host. © 2011 Entomological Society of America.