Cyanobacterial protease inhibitors lead to maternal transfer of increased protease gene expression in Daphnia

Protease inhibitors (PIs) have frequently been found in cyanobacterial blooms and have been shown to affect the major herbivore Daphnia by decreasing growth and inhibiting gut protease activity. However, it has been shown that a clone of Daphnia is able to respond to dietary PIs by increasing its protease gene expression. Such an inducible response might be maternally transferred to the next generation. Therefore, we tested a tolerant clone for maternal transfer of protease gene expression. When exposed to the trypsin inhibitor-producing cyanobacterium Microcystis aeruginosa PCC7806 Mut, Daphnia mothers and their untreated newborns showed an increase in trypsin gene expression compared to naïve mothers grown on control food and their offspring. The maternally transferred increase in gene expression was accompanied by a higher somatic growth rate of the offspring generation from exposed mothers compared to offspring from naïve mothers. This higher growth rate compensated for the lower dry mass of newborns from exposed mothers and led to the same fitness as observed in the offspring of naïve mothers. In nature, clones that can maternally transfer increased protease gene expression should have an advantage over clones that cannot. The selection for such more tolerant clones by naturally occurring PIs might lead to microevolution of natural Daphnia populations, and to local adaptation in the long term. This is the first study to show an adaptive maternal transfer of increased target gene expression in an ecological context.