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Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Abstract

The information about the magnitude of differences in thermal plasticity both between and within populations, as well as identification of the underlying molecular mechanisms are key to understanding the evolution of thermal plasticity. In particular, genes underlying variation in the physiological response to temperature can provide raw material for selection acting on plastic traits. Using RNAseq, we investigate the transcriptional response to temperature in males and females from bulb mite populations selected for the increased frequency of one of two discrete male morphs (fighter- and scrambler-selected populations) that differ in relative fitness depending on temperature. We show that different mechanisms underlie the divergence in thermal response between fighter- and scrambler-selected populations at decreased vs. increased temperature. Temperature decrease to 18 °C was associated with higher transcriptomic plasticity of males with more elaborate armaments, as indicated by a significant selection-by-temperature interaction effect on the expression of 40 genes, 38 of which were upregulated in fighter-selected populations in response to temperature decrease. In response to 28 °C, no selection-by-temperature interaction in gene expression was detected. Hence, differences in phenotypic response to temperature increase likely depended on genes associated with their distinct morph-specific thermal tolerance. Selection of males also drove gene expression patterns in females. These patterns could be associated with temperature-dependent fitness differences between females from fighter- vs. scrambler-selected populations reported in previous studies. Our study shows that selection for divergent male sexually selected morphologies and behaviors has a potential to drive divergence in metabolic pathways underlying plastic response to temperature in both sexes.

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Fig. 1: Schematic representation of the experimental design.
Fig. 2: Overview of genes with differential expression between selection treatments and genes showing selection-by-temperature interaction in expression.
Fig. 3: Venn diagrams with numbers of differentially expressed genes for different temperatures in males and females.
Fig. 4

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Acknowledgements

We thank Genomics and Experimental Evolution Group members (Jagiellonian University), Aleksandra Walczyńska (Jagiellonian University), Jacek Radwan (Adam Mickiewicz University) and three anonymous reviewers for their comments on the previous version of the manuscript. The study was funded by a grant from Polish National Science Centre awarded to Agata Plesnar-Bielak, grant no UMO-2015/19/B/NZ8/01393. Experimental populations were established as a part of Jacek Radwan’s project financed from National Science Centre. Part of the computations were performed at the Poznan Supercomputing and Networking Centre.

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APB, MK and WB designed the study, JP, SC and AŁ established and maintained experimental evolution populations, APB, KD and MM performed experiments, KD and WB consulted molecular methods, APB and MK analyzed the data, APB, MK and WB wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Agata Plesnar-Bielak.

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Plesnar-Bielak, A., Parrett, J.M., Chmielewski, S. et al. Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait. Heredity 133, 43–53 (2024). https://doi.org/10.1038/s41437-024-00691-4

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