The genomic footprint of climate adaptation in Chironomus riparius

Abstract

The gradual heterogeneity of climatic factors poses varying selection pressures across geographic distances that leave signatures of clinal variation in the genome. Separating signatures of clinal adaptation from signatures of other evolutionary forces, such as demographic processes, genetic drift and adaptation, to nonclinal conditions of the immediate local environment is a major challenge. Here, we examine climate adaptation in five natural populations of the harlequin fly Chironomus riparius sampled along a climatic gradient across Europe. Our study integrates experimental data, individual genome resequencing, Pool-Seq data and population genetic modelling. Common-garden experiments revealed significantly different population growth rates at test temperatures corresponding to the population origin along the climate gradient, suggesting thermal adaptation on the phenotypic level. Based on a population genomic analysis, we derived empirical estimates of historical demography and migration. We used an F outlier approach to infer positive selection across the climate gradient, in combination with an environmental association analysis. In total, we identified 162 candidate genes as genomic basis of climate adaptation. Enriched functions among these candidate genes involved the apoptotic process and molecular response to heat, as well as functions identified in studies of climate adaptation in other insects. Our results show that local climate conditions impose strong selection pressures and lead to genomic adaptation despite strong gene flow. Moreover, these results imply that selection to different climatic conditions seems to converge on a functional level, at least between different insect species.

Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum)

“…Similar to our finding of a dominating effect of mean annual temperature on landscape genetic connectivity, temperature was associated with the highest number of SNPs under putative selection in P. vittatum . Our results are consistent with other studies that have reported (via EAA and outlier tests) a key role of temperature in driving adaptive genetic differentiation in insects (e.g., Dudaniec et al, ; Feng et al, ; Waldvogel et al, ), and in other systems (e.g., trees: Jordan, Hoffmann, Dillon, & Prober, ; vertebrates: Manthey & Moyle, ; marine invertebrates: Xuereb, Kimber, Curtis, Bernatchez, & Fortin, ).…”

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

“…This temperature is just below the upper sustainable temperature limit of the species, as inferred from previous experiments and presented a priori a substantial selection pressure (Foucault, Wieser, Waldvogel, Feldmeyer, et al, ; Nemec et al, ). This may be particularly true for this rather cold adapted, Northern population (Waldvogel et al, ). Apart from the experimental temperatures, rearing conditions regarding food availability, air humidity, etc., were a priori kept as selectively lenient as possible.…”

“…Whole genome pool‐sequencing was carried out on an Illumina MySeq with 250 bp paired end reads. Reads were trimmed using the wrapper tool autotrim (Waldvogel et al, ) that integrates trimmomatic (Bolger, Lohse, & Usadel, ) for trimming and fastQC (Andrews, ) for quality control. The trimmed reads were then mapped on the latest C. riparius reference genome (Schmidt et al, ) using the BWA mem algorithm (Li & Durbin, ).…”

“…Nemec, Patel, Nowak, and Pfenninger () showed that population growth rate (PGR, a composite fitness measure of several phenotypic fitness traits, see below) varied among five natural C. riparius populations sampled across a climatic gradient in Europe when subjected to three temperature treatments in a full factorial common garden experiment. In a recent study, it has been shown that populations of C. riparius from across the species range are indeed adapted to their locale climate and that the genetic basis of this adaptation involves many loci across the genome (Waldvogel et al, ). Additionally, an experimental evolution indicated that such an adaptive phenotypic reaction to temperature treatments may be extremely rapid in this species (Foucault, Wieser, Waldvogel, Feldmeyer, & Pfenninger, ).…”

Establishing laboratory cultures and performing ecological and evolutionary experiments with the emerging model species Chironomus riparius

“…Moreover, the integration of experimental investigations with genetics and genomics is possible since the publication of a high‐quality draft genome as reference sequence (Oppold et al, ). Furthermore, important population genetic parameters have been studied, such as the species‐specific spontaneous mutation rate (Oppold & Pfenninger, ), its genomic and transcriptomic basis of niche differentiation (Schmidt, Greshake, Feldmeyer, Hankeln, & Pfenninger, ), demography in European populations (Waldvogel et al, ), and its genomic architecture (Kraemer & Schmidt, ; Oppold et al, ; Zampicinini, Blinov, Cervella, Guryev, & Sella, ). The possibility to easily obtain natural populations from a large distribution range, its capacity to cope with laboratory culture conditions and the availability of genetic and genomic resources makes C. riparius a suitable study organism for many disciplines and research areas.…”