Trade-offs during the development of primary and secondary sexual traits in a horned beetle

摘要

Resource allocation trade-offs during development affect the final sizes of adult structures and have the potential to constrain the types and magnitude of evolutionary change that developmental processes can accommodate. Such trade-offs can arise when two or more body parts compete for a limited pool of resources to sustain their growth and differentiation. Recent studies on several holometabolous insects suggest that resource allocation trade-offs may be most pronounced in tissues that grow physically close to each other. Here we examine the nature and magnitude of developmental trade-offs between two very distant body parts: head horns and genitalia of males of the horned scarab beetle Onthophagus taurus. Both structures develop from imaginal disklike tissues that undergo explosive growth during late larval development but differ in exactly when they initiate their growth. We experimentally ablated the precursor cells that normally give rise to male genitalia at several time points during late larval development and examined the degree of horn development in these males compared to that of untreated and sham-operated control males. We found that experimental males developed disproportionately larger horns. Horn overexpression was weakest in response to early ablation and most pronounced in males whose genital disks were ablated just before larvae entered the prepupal stage. Our results suggest that even distant body parts may rely on a common resource pool to sustain their growth and that the relative timing of growth may play an important role in determining whether, and how severely, growing organs will affect each other during development. We use our findings to discuss the physiological causes and evolutionary consequences of resource allocation trade-offs.