“The evolutionary ecology of metamorphosis”

Posted on

Hanna ten Brink, André M. de Roos, and Ulf Dieckmann (May 2019)

The DOI will be https://dx.doi.org/10.1086/701779

Why is metamorphosis widespread in the animal kingdom, despite a few evolutionary origins? It is an evolutionary trap!

The evolutionary ecology of metamorphosis

A newly emerged monarch butterfly (Danaus plexippus).
(Image © Jan van Arkel, IBED/University of Amsterdam)

A butterfly slowly emerges from its chrysalis, revealing its colorful wings. Not that long ago, this butterfly was a fat caterpillar, gorging itself on juicy leaves. It then molted into a pupa, ready to metamorphose itself into an elegant butterfly. Metamorphosis occurs not only in butterflies, but in the majority of all animal species. Why has metamorphosis evolved and why is it so pervasive in the animal kingdom?

In this study, ten Brink, de Roos, and Dieckmann show with a mathematical model that metamorphosis can only evolve under limited ecological conditions. During metamorphosis, individuals rebuild their body plan. The benefit of this is that larvae and adults have different morphologies, each specialized in feeding on different food types. Metamorphosis is, however, energetically very costly and also dangerous (a pupa can, for example, not run away from a predator). Metamorphosis will therefore only evolve when the benefits of having a metamorphosis are very high. This is the case when individuals have access to an abundant food source after metamorphosis.

Surprisingly, the researchers find that species with a metamorphosis will not abandon this life-history strategy when the ecological conditions change under which metamorphosis initially evolved. The reason for this is that individuals are, after metamorphosis, not very efficient in feeding on the food source they ate as larvae. Metamorphosed individuals can therefore not easily switch back to this larval food source in case the food type they feed on becomes scarce. Instead, there is selection to become even more specialized in feeding on this limited food, resulting in a more pronounced metamorphosis and more dissimilar life-stages. The findings in this study can explain the widespread occurrence of metamorphosis, despite only a few evolutionary origins.


Abstract

Almost all animal species undergo metamorphosis, even though empirical data show that this life-history strategy evolved only a few times. Why is metamorphosis so widespread and why has it evolved? Here we study the evolution of metamorphosis using a fully size-structured population model in conjunction with the adaptive-dynamics approach. We assume that individuals compete for two food sources, one of these, the primary food source, is available to individuals of all sizes. The secondary food source is available only to large individuals. Without metamorphosis, unresolvable tensions arise for species faced with the opportunity of specializing on such a secondary food source. We show that metamorphosis can evolve as a way to resolve these tensions, such that small individuals specialize on the primary food source, while large individuals specialize on the secondary food source. We find, however, that metamorphosis only evolves when the supply rate of the secondary food source exceeds a high threshold. Individuals postpone metamorphosis when the ecological conditions under which metamorphosis originally evolved deteriorate but will often not abandon this life-history strategy, even if it causes population extinction through evolutionary trapping. In summary, our results show that metamorphosis is not easy to evolve but, once evolved, it is hard to lose. These findings can explain the widespread occurrence of metamorphosis in the animal kingdom despite its few evolutionary origins.