Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures

Abstract

Evolve and Resquence (E&R) studies are a useful tool to study genomic processes during rapid adaptation, e.g., in the framework of adaptive responses to global climate change. We applied different thermal regimes to a natural Chironomus riparius (Diptera) population in an E&R framework to infer its evolutionary potential for rapid thermal adaptation. We exposed two replicates to three temperatures each (14°C, 20°C and 26°C) for more than two years, the experiment thus lasting 22, 44 or 65 generations, respectively. The two higher temperatures presented a priori moderate, respectively strong selection pressures. Life‐cycle fitness tests revealed no appreciable adaptation to thermal regimes but a common adaptation of all six replicates probably due to the rearing conditions, presumably increased larval density and water quality. Genomic analyses showed a strong, genome‐wide selective response in all replicates (mean s of selected SNPs = 0.305). This genomic response was significantly similar at all genomic levels among all replicates (SNPs, 10 kb windows, genes, exons, regions of elevated allele frequency change [REA]). The intersections among the replicates exposed to the same temperature were either insignificant or underrepresented. This confirmed a selective response to identical selection pressure(s), however, not to thermal regime. Genes closest to the SNP with the highest selection coefficient per REA were enriched for GO terms related to ion transport, regulation of transcription and signal transduction, which supported the presumed acting selection pressures. Our study showed the evolutionary potential for rapid adaptation by genome‐wide and probably polygenic selection on standing genetic variation in C. riparius. However, because of the impossibility to accurately predict the acting selective regime in evolutionary experiments, we discuss the sobering perspectives for inferring the evolutionary potential of natural populations with this approach.

Parallel gene expression evolution in natural and laboratory evolved populations

“…An interesting comparison with our results is an E&R study of Chironomus riparius populations which shared the same genomic response despite having evolved under different temperature regimes (Pfenninger & Foucault, 2020). In this study, we also identified some gene expression changes common to both temperature regimes (Figure 3), highlighting the impact of laboratory environment on expression levels.…”

Measuring mutagenicity in ecotoxicology: A case study of Cd exposure inChironomus riparius

“…Its genome was recently sequenced and annotated, enabling more complex genomic studies (Oppold et al, 2017; Schmidt et al, 2020). Moreover, it is known that C. riparius can rapidly adapt to environmental stress (Nowak et al, 2009; Pfenninger and Foucault, 2020).…”

Can laboratory evolution experiments teach us about natural populations?

“…However, not all such efforts are so successful. In fact, a recent, very similar article recently published in Molecular Ecology concluded that E&R results from experiments with the harlequin fly ( Chironomus riparius ) were not relevant to the study of thermal adaptation in natural populations of this species (Pfenninger & Foucault, 2020). Here, the authors found no evidence of temperature‐specific changes in patterns of genetic variation across selection treatments (control, intermediate and high temperature) and concluded their study could not provide direct insights into the potential for thermal adaptation in natural C. riparius populations.…”

“…Perhaps laboratory evolution experiments fail to comprehensively mimic the environments that natural populations encounter. Pfenninger and Foucault (2020) sought to use experimental evolution to assess the evolutionary potential for rapid thermal adaptation in natural C . riparius populations, but the general laboratory environment proved a much stronger selective agent than any of the thermal treatments.…”