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Can synergistic pleiotropy explain the low parallelism of temperature mediated gene expression evolution?


Authors:
Dagny A. Runarsdottir 1,2; Viola Nolte 1; Christian Schlötterer 1

Affiliations:
1) Institute of population genetics, University of Veterinary Medicine, Vienna, Austria; 2) Vienna graduate school of population genetics, Vienna, Austria

Keywords:
Experimental evolution

Parallel phenotypic responses to similar environmental stressors have been described not only for different populations, but also between species. Since many of these traits are highly complex, it is not clear to what extent this parallel evolution can be also seen on the molecular level. Here, we address this question by studying the transcriptomic response of polymorphic founder populations from two species, Drosophila melanogaster and D. simulans to controlled laboratory conditions with fluctuating high (18/28°C) and low (10/20°C) temperature regimes. In both species a strong adaptive response towards temperature in gene expression was observed. 193 genes were differently expressed (DE) between high and low temperature for D. melanogaster and 189 for D. simulans. Only two (Jaccard index = 0.01) and five (J.I. = 0.03) up- and downregulated genes, respectively, were shared between the species. Additionally, a correlation of the overall transcriptome responses was low (Spearman’s rho = -0.067). Despite the lack of parallel responses on the level of individual genes, the evolved genes in both species were enriched among midgut and accessory gland specific genes (J.I. = 0.67). Understanding how the experimental thermal adaptation we observe in this study is reflected in natural population is important, especially with temperature being one of the most important environmental stressors. Comparing clinal evolution to experimental thermal evolution of the same species provides a valuable information on this matter. Interestingly, the two species differed in the extent to which the same genes evolved in the laboratory and natural populations. While D. melanogaster shared more genes than expected by chance, no shared response was detected for D. simulans, which could be explained by the different demographies of the species. Reasoning that pleiotropy may be a major factor determining the adaptive gene expression evolution, we compared the levels of pleiotropy among the significant genes of all four groups. In natural populations, pleiotropy appeared to be higher than in the laboratory, for both species. This might be explained by the more complex environments in the wild (synergistic pleiotropy). We propose that pleiotropy may be an important, but complex, factor contributing to the repeatability of gene expression evolution.