A mountain fly’s eye view of climate warming: laboratory evolution experiments

Mountains are hot spots of biodiversity, this biodiversity being especially vulnerable to rapid climate warming. In particular for organisms in higher altitudes, the potential to shift their distribution upwards to cooler habitats will often be limited. For these species, only rapid evolution of the ecological niche would offer a long-time solution. The aim of this project is to explore evolutionary and ecological effects of rising temperature on mountain biodiversity at the phenotypic and genotypic level, using the cool-climate mountain fly Drosophila nigrosparsa as a laboratory-evolution system. We propose to expose the fly to rising temperature according to the worst-case scenario predicted for ten years locally, and to test six hypotheses (H1-H6) relating to three questions. Extent of thermal evolution? A population can only persist in situ if the extent and tempo of temperature increase is matched by the extent and tempo of adaptive evolution. For some habitat specialists, little potential for adaptation to climate change was found. Using laboratory selection, we will test whether thermal-niche evolution in D. nigrosparsa is (H1) insufficient vs. (H2) sufficient. H1 would likely imply that the fly would shift upwards or would disappear from mountains too low in elevation, H2 that it could in principle maintain its current distribution. To validate the ecological relevance of our lab results, we will do field cage tests. Costs of thermal evolution? Selection for one trait often comes at the cost of reduced other fitness components. On the other hand, evidence suggests this may not necessarily be the case with adaptation to rising temperature in insects. Considering cold resistance, productivity, competitive ability, and starvation resistance, we will thus evaluate whether adaptation to rising temperature (H3) imposes vs. (H4) does not impose costs in our fly. Genetics of thermal evolution? Deciphering the genetics of adaptation to changing environments is core to evolutionary ecology. We will use next-generation genome sequencing of pooled individuals for genome-wide searches for putative selection signatures at the nucleotide level. The number of selection signatures will be of interest in their own right. We will also use the distribution of selection signatures across the genome to test the non-exclusive hypotheses that evolution occurred in (H5) coding or (H6) non-coding stretches. For putative selection signatures in genes, we will compare their functional annotations to the results from other topical studies. The project is one starting point in exploring if and how populations and, ultimately, the species may survive climate warming. The project will be relevant also beyond its specific aims: The answers to the questions addressed will facilitate a range of follow-up research and will broaden the basis of empirical data on the evolutionary potential across taxa. The study will be important as a case study that uses the emerging approach of genome sequencing of pooled individuals. The field cage test is innovative in assessing the ecological relevance of lab- selection findings without altering natural populations. Identifying potential costs of thermal evolution will, together with the results from other studies, be useful in the context of designing management programmes for minimising biodiversity loss under rapid climate change. Information about what loci harbour selection signatures in our species will contribute to identifying general patterns in thermal-evolution and stress-research genomics and will add insight into the hotly debated relative contributions of coding vs. non-coding, regulatory regions to adaptation.

Mountain biodiversity has been considered especially vulnerable to climate change. However, no Alpine study system has been available for experimental evolution to predict the future fate of mountain organisms. We exposed the mountain fly Drosophila nigrosparsa to rising temperature according to local predictions. We found that the fly is not able to improve its heat resistance by evolution, at least not in the speed made necessary by the current rise of temperature. It even suffers from reduced heat resistance and competitive ability when reared under increased temperature. In essence, the fly will likely lose parts of its current distribution if temperature continues to rise. In establishing the new study system, we characterised its life history, physiological limits, and genome. The fly breeds on fungi; this specialisation likely was made possible by changes in the flys olfaction that were imprinted in its genome. Compared with other Drosophila species, D. nigrosparsa is less fecund, relatively long-living, starvation susceptible, cold adapted, and relatively well tolerant to brief heat peaks. Our results highlight the importance of (i) basic life-history research for the interpretation of results from other fields, (ii) climate-change biology for predicting the impacts on an Alpine study system, and of (iii) combining the study of the genome and the protein structure encoded in the genome for identifying evolutionary trajectories including in non-model organisms.