Rapid growth and the evolution of complete metamorphosis in insects.

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.

Complete metamorphosis and microbiota turnover in insects.

The insects constitute the majority of animal diversity. Most insects are holometabolous: during complete metamorphosis their bodies are radically reorganized. This reorganization poses a significant challenge to the gut microbiota, as the gut is replaced during pupation, a process that does not occur in hemimetabolous insects. In holometabolous hosts, it offers the opportunity to decouple the gut microbiota between the larval and adult life stages resulting in high beta diversity whilst limiting alpha diversity. Here, we studied 18 different herbivorous insect species from five orders of holometabolous and three orders of hemimetabolous insects. Comparing larval and adult specimens, we find a much higher beta-diversity and hence microbiota turnover in holometabolous insects compared to hemimetabolous insects. Alpha diversity did not differ between holo- and hemimetabolous insects nor between developmental stages within these groups. Our results support the idea that pupation offers the opportunity to change the gut microbiota and hence might facilitate ecological niche shifts. This possible effect of niche shift facilitation could explain a selective advantage of the evolution of complete metamorphosis, which is a defining trait of the most speciose insect taxon, the holometabola.

Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia).

Parasites are rarely included in food web studies, although they can strongly alter trophic interactions. In aquatic ecosystems, poorly grazed cyanobacteria often dominate phytoplankton communities, leading to the decoupling of primary and secondary production. Here, we addressed the interface between predator-prey and host-parasite interactions by conducting a life-table experiment, in which four Daphnia galeata genotypes were maintained on quantitatively comparable diets consisting of healthy cyanobacteria or cyanobacteria infected by a fungal (chytrid) parasite. In four out of five fitness parameters, at least one Daphnia genotype performed better on parasitised cyanobacteria than in the absence of infection. Further treatments consisting of purified chytrid zoospores and heterotrophic bacteria suspensions established the causes of improved fitness. First, Daphnia feed on chytrid zoospores which trophically upgrade cyanobacterial carbon. Second, an increase in heterotrophic bacterial biomass, promoted by cyanobacterial decay, provides an additional food source for Daphnia. In addition, chytrid infection induces fragmentation of cyanobacterial filaments, which could render cyanobacteria more edible. Our results demonstrate that chytrid parasitism can sustain zooplankton under cyanobacterial bloom conditions, and exemplify the potential of parasites to alter interactions between trophic levels.