The genomic footprint of climate adaptation inChironomus riparius

Abstract

The gradual heterogeneity of climatic factors pose 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 non-clinal 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 a positive correlation of population growth rates 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 ST 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 other 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.

Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world

“…Therefore, under a global warming scenario, rolled‐leaf beetles are severely threatened at high elevations, as there are no colder upland habitats to disperse to, whereas Drosophila species depend strongly on access to habitats to which they are preadapted (Kellermann et al ., ; García‐Robledo et al ., ). Genomic evidence is already identifying candidate genes for adaptation to climatic gradients in natural populations considering that not only tolerance to heat, but also to precipitation, cold and other environmental factors can be under strong selection (Waldvogel et al ., ). In general, although genetic adaptation in response to climate change has been observed in some insects and may result from rapid evolution (Barghi et al ., ), the evidence is still scarce (e.g.…”

Evolutionary genomics can improve prediction of species’ responses to climate change

“…; Chironomus riparius , Waldvogel et al. ), molluscs ( Crassostrea gigas , Zhang et al. ), and vertebrates (domesticated sheep, Yang et al.…”

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

“…To monitor overall population fitness, we estimate the population growth rate (PGR) in a standardized Life cycle Fitness Test (LCFT) (OECD, ; Waldvogel et al, ) with modifications. A group of individuals of the same population is exposed to the parameters or stressors of interest over their entire lifespan.…”

“…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.…”