Thermal tolerance in the keystone species Daphnia magna—a candidate gene and an outlier analysis approach

Abstract

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long-term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm- and cold-adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST-linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.

Population transcriptomics in Daphnia: The role of thermal selection

“…A phylogeographic signal explains the lower amount of DNA sequence and expression divergence observed among Lake Constance and other populations. It is also in accordance with a recent study on D. magna that demonstrated little change in population structure even following severe artificial selection (Jansen et al., ).…”

“…A comparable observation was made by Jansen et al. (), who analysed subpopulations of D. magna across time (utilizing qPCR and a resurrection ecology approach) and reported loss of plasticity in expression levels under evolutionary constraints in a large proportion of temperature candidate genes.…”

Temperature gradient affects differentiation of gene expression and SNP allele frequencies in the dominant Lake Baikal zooplankton species

“…To evaluate the enrichment of transcripts showing a significant DE or possessing outlier SNP sites with orthologs of genes previously identified as candidate genes involved in thermal acclimation or adaptation (cf Jansen et al., ), we matched the approach of Herrmann, Ravindran, Schwenk, and Cordellier (). Specifically, we identified the list of orthologous groups (OGs) identified among E. baikalensis transcripts by orthomcl (Fischer et al., ) with the OGs of arthropod genes previously identified as candidate thermal adaptation genes.…”

Thermal evolution offsets the elevated toxicity of a contaminant under warming: A resurrection study in Daphnia magna

“…This can be expected because when a population evolves tolerance to a certain stressor that environmental condition is no longer experienced as a stressor (Vam Straalen, 2003). With regard to warming, the acquisition of genetic adaptation to higher temperatures has been demonstrated in several taxa and has been linked to changes in gene expressions (e.g., Garvin, Thorgaard, & Narum, 2015; Gleason & Burton, 2015; Narum, Campbell, Meyer, Miller, & Hardy, 2013; Porcelli, Butlin, Gaston, Joly, & Snook, 2015; for the study species: Jansen et al., 2017; Yampolsky et al., 2014). Thermal evolution is expected to reduce the energetic costs of dealing with warming, thus leaving more energy to deal with stressors such as toxicants, thereby potentially offsetting the synergism between the toxicant and warming.…”