Complex life cycles: why refrain from growth before reproduction in the adult niche?

Organisms with complex life cycles occupy distinct niches as larvae and adults. One presumed advantage of this is the ability to exploit different resources successively throughout ontogeny. Various taxa, however, have evolved nonfeeding, nongrowing adult stages. We show theoretically that this counterintuitive no growth strategy is favored when the optimal larval size is greater than or equal to the optimal adult size for reproduction. We empirically investigated this in a group of parasitic worms (helminths). Helminths are transmitted trophically between hosts before reproducing in large, high-trophic-level hosts, and most undergo considerable growth as adults in their final host. Some well-studied tapeworm species (Schistocephalus, Ligula, and Digramma species) are notable exceptions; they reproduce semelparously without any growth in their final habitat (the gut of piscivorous birds). Using cross-species comparative analyses, we show that these tapeworms that do not grow in their final host (1) attain larval sizes in their last intermediate host (fishes) that are comparable to or larger than the adult sizes reached by tapeworms that do grow in the same adult niche (also piscivorous birds) and (2) are large, even as larvae, relative to the mass of their final hosts. These results are consistent with the idea that a massive larval size can make adult growth superfluous, and we discuss whether this likely applies to other complex life cycle taxa with nonfeeding, nongrowing adults.