Selective effects of a short transient environmental fluctuation on a natural population.

Natural populations experience continuous and often transient changes of environmental conditions. These in turn may result in fluctuating selection pressures leading to variable demographic and evolutionary population responses. Rapid adaptation as short-term response to a sudden environmental change has in several cases been attributed to polygenic traits, but the underlying genomic dynamics and architecture are poorly understood. In this study, we took advantage of a natural experiment in an insect population of the non-biting midge Chironomus riparius by monitoring genome-wide allele frequencies before and after a cold snap event. Whole genome pooled sequencing of time series samples revealed 10 selected haplotypes carrying ancient polymorphisms, partially with signatures of balancing selection. By constantly cold exposing genetically variable individuals in the laboratory, we could demonstrate with whole genome resequencing (i) that among the survivors, the same alleles rose in frequency as in the wild, and (ii) that the identified variants additively predicted fitness (survival time) of its bearers. Finally, by simultaneously sequencing the genome and the transcriptome of cold exposed individuals we could tentatively link some of the selected SNPs to the cis- and trans-regulation of genes and pathways known to be involved in cold response of insects, such as cytochrome P450 and fatty acid metabolism. Altogether, our results shed light on the strength and speed of selection in natural populations and the genomic architecture of its underlying polygenic trait. Population genomic time series data thus appear as promising tool for measuring the selective tracking of fluctuating selection in natural populations.

Population Genomic Time Series Data of a Natural Population Suggests Adaptive Tracking of Fluctuating Environmental Changes.

Natural populations are constantly exposed to fluctuating environmental changes that negatively affect their fitness in unpredictable ways. While theoretical models show the possibility of counteracting these environmental changes through rapid evolutionary adaptations, there have been few empirical studies demonstrating such adaptive tracking in natural populations. Here, we analyzed environmental data, fitness-related phenotyping and genomic time-series data sampled over 3 years from a natural Chironomus riparius (Diptera, Insecta) population to address this question. We show that the population's environment varied significantly on the time scale of the sampling in many selectively relevant dimensions, independently of each other. Similarly, phenotypic fitness components evolved significantly on the same temporal scale (mean 0.32 Haldanes), likewise independent from each other. The allele frequencies of 367,446 SNPs across the genome showed evidence of positive selection. Using temporal correlation of spatially coherent allele frequency changes revealed 35,574 haplotypes with more than one selected SNP. The mean selection coefficient for these haplotypes was 0.30 (s.d. = 0.68). The frequency changes of these haplotypes clustered in 46 different temporal patterns, indicating concerted, independent evolution of many polygenic traits. Nine of these patterns were strongly correlated with measured environmental variables. Enrichment analysis of affected genes suggested the implication of a wide variety of biological processes. Thus, our results suggest overall that the natural population of C. riparius tracks environmental change through rapid polygenic adaptation in many independent dimensions. This is further evidence that natural selection is pervasive at the genomic level and that evolutionary and ecological time scales may not differ at all, at least in some organisms.

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

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.

Rapid adaptation to high temperatures in Chironomus riparius.

Effects of seasonal or daily temperature variation on fitness and physiology of ectothermic organisms and their ways to cope with such variations have been widely studied. However, the way multivoltines organisms cope with temperature variations from one generation to the next is still not well understood. The aim of this study was to investigate whether the multivoltine midge Chironomus riparius Meigen (1803) responds mainly via acclimation as predicted by current theories or whether rapid genetic adaptation is involved. To investigate this issue, a common garden approach has been applied. A mix of larvae from five European populations was raised in the laboratory at three different pre-exposure temperatures (PET): 14, 20, and 26°C. After three and five generations, respectively, larvae were exposed to three treatment temperatures (TT): 14, 20, and 26°C. Mortality was monitored for the first 48 hr and after emergence. After three generations, significant mortality rate differences depended on an interaction of PET and TT. This finding supports the hypothesis that chironomids respond rapidly to climatic variation via adaptive mechanisms and to a lesser extent via phenotypic plasticity. The result of the experiment indicates that three generations were sufficient to adapt to warm temperature, decreasing the mortality rate, highlighting the potential for chironomids to rapidly respond to seasonally changing conditions.