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

• Published in: Molecular ecology Vol. 32; no. 2; pp. 335 - 349
• Main Authors: Pfenninger, Markus, Foucault, Quentin, Waldvogel, Ann‐Marie, Feldmeyer, Barbara
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.01.2023
• Subjects: Adaptation, Physiological - genetics; Alleles; Biological Evolution; Cold; Cytochrome; Cytochrome P450; Cytochromes P450; Environmental changes; Environmental conditions; Fatty acids; fluctuating selection; Gene frequency; Gene Frequency - genetics; Gene regulation; Gene sequencing; Genomes; Genomics; genotype–phenotype map; Haplotypes; Humans; Insects; Metabolism; Natural populations; Polygenic inheritance; Polymorphism, Single Nucleotide - genetics; Population; Populations; Selection, Genetic; selective tracking; Single-nucleotide polymorphism; Time series; Transcriptomes; genotype-phenotype map; fluctuating selection; selective tracking
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.16748

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.