Rapid growth and the evolution of complete metamorphosis in insects

Christin Manthey, C. Jessica E. Metcalf , Michael T. Monaghan , Ulrich K. Steiner,  and Jens Rolff

PNAS September 9 2024; 121 (38) e2402980121. EVOLUTION

Significance

More than half of all animal species are insects that undergo a dramatic rebuilding of their bodies, dubbed complete metamorphosis, as exemplified by the transition from a caterpillar through a pupa to a butterfly. Why this extreme lifestyle evolved is unclear. Here, by combining empirical data and mathematical modeling, we find that the holometabolous insects grow much faster than insects that do not show this extreme form of metamorphosis. This allows to first grow and then build the adult body, allowing for much faster growth. Fast growth is favorable under many ecological conditions such as competition and predation. This growth advantage reported here can almost certainly help to understand the huge diversification of the holometabolous insects.

Abstract

More than 50% of all animal species are insects that undergo complete metamorphosis. The key innovation of these holometabolous insects is a pupal stage between the larva and adult when most structures are completely rebuilt. Why this extreme lifestyle evolved is unclear. Here, we test the hypothesis that a trade-off between growth and differentiation explains the evolution of this novelty. Using a comparative approach, we find that holometabolous insects grow much faster than hemimetabolous insects. Using a theoretical model, we then show how holometaboly evolves under a growth-differentiation trade-off and identify conditions under which such temporal decoupling of growth and differentiation is favored. Our work supports the notion that the holometabolous life history evolved to remove developmental constraints on fast growth, primarily under high mortality.

See https://www.pnas.org/doi/10.1073/pnas.2402980121

Figure 2: Schematic of the model. Organisms can adopt a holometabolous (Top) or hemimetabolous (Bottom) life cycle. In the former, a period of growth in size (accumulation of blue bricks), is followed by a period of differentiation (accumulation of red bricks, simplified to r3 in the model, as there are limited data to inform rates of mortality over the duration of differentiation Δ, see SI Appendix). The parameter k describes background allocation to growth that is always present; r₁ quantifies the flexible resource allocation toward growth that could also be allocated to differentiation. For hemimetabolous life cycles, differentiation can also occur during the growth phase (pink bricks, lower row), by allocation of r2 resources. This reduces resources available for the rate of growth in size (grayed-out bricks, Upper row). During the final life phase in a hemimetabolous life cycle, remaining resources, r3, can be used to make up remaining differentiation possible, r3e-r2t-v. For the holometabolous life cycle, since r₂ = 0, this reduces to r3. The total resources pool is constrained such that r1+r2+r3=1 (schematic, Right). Growth and differentiation are combined to define fertility, and this is multiplied by survival during the growth phase to define fitness. We estimate fitness across the full spectrum of possible values of r₁ and r₂ (which in turn define r₃), as well as a wide range of durations of the growth phase t allow us to identify the optimal life histories, and discriminate parameter combinations where the optimal r₃ = 0 (which corresponds to hemimetabola) from those where the optimal r₃ > 0 (corresponding to holometabola).