Positive selection of digestive proteases in Daphnia: A mechanism for local adaptation to cyanobacterial protease inhibitors.

Anke Schwarzenberger,Martin Hasselmann,Eric Von Elert

doi:10.1111/mec.15375

Anke Schwarzenberger, Martin Hasselmann + Show 1 more

Open Access

https://doi.org/10.1111/mec.15375

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Abstract

Due to the combined effects of global warming and eutrophication, the frequency of deleterious cyanobacterial blooms in freshwater ecosystems has increased. In line with this, local adaptation of the aquatic keystone herbivore Daphnia to cyanobacteria has received major attention. Besides microcystins, the most frequent cyanobacterial secondary metabolites in such blooms are protease inhibitors (PIs). Recently, it has been shown that a protease gene showed copy number variation between four D.magna populations that differed in tolerance to PIs. From that study, we chose two distinct populations of D.magna which had or had not coexisted with cyanobacteria in the past. By calculating FST values, we found that the two populations were genetically more distant in the protease loci than in neutral loci. Population genetic tests applied to the tolerant population revealed that positive selection was most probably acting on the gene loci of the digestive protease CT448 and CT802. We conclude that the selection of digestive proteases and subsequent reduction in copy number is the molecular basis of evolutionary changes leading to local adaptation to PIs.

Highlights

Adaptations – locally and over time – have been observed in both terrestrial and aquatic ecosystems
Schwarzenberger, Keith, Jackson, and Von Elert (2017) have demonstrated that four distinct D. magna populations differed in tolerance to dietary chymotrypsin inhibitors, and that this difference in tolerance corresponded with the cyanobacterial history of the populations’ lakes of origin which hints at local adaptation
Digestive proteases in the gut of Daphnia are inhibited by cyanobacterial protease inhibitors

Summary

| INTRODUCTION

Adaptations – locally and over time – have been observed in both terrestrial and aquatic ecosystems. Schwarzenberger, Keith, Jackson, and Von Elert (2017) have demonstrated that four distinct D. magna populations differed in tolerance to dietary chymotrypsin inhibitors, and that this difference in tolerance corresponded with the cyanobacterial history of the populations’ lakes of origin which hints at local adaptation. Only three trypsin and three chymotrypsin genes (i.e., CT383, CT448 and CT802) were assigned to the proteases active in the gut of D. magna (Schwarzenberger et al, 2010) One of those chymotrypsin genes, i.e., CT448, was demonstrated to show copy number variation with fewer copies in a more tolerant population (Schwarzenberger et al, 2017). The three chymotrypsin genes and especially CT448 are likely to be the targets of selection, and might constitute the genetic basis underlying local adaptation of Daphnia populations to chymotrypsin inhibitors. In a population genetic approach, we calculated the genetic distances between the two populations and investigated whether the chymotrypsin genes of the tolerant population had been selected

| MATERIALS AND METHODS

Findings

| DISCUSSION