The strength and form of natural selection on transcript abundance in the wild

Gene transcription variation is known to contribute to disease susceptibility and adaptation, but we currently know very little about how contemporary natural selection shapes transcript abundance. Here, we propose a novel analytical framework to quantify the strength and form of ongoing natural selection at the transcriptome level in a wild vertebrate. We estimated selection on transcript abundance in a cohort of a wild salmonid fish (Salmo trutta) affected by an extracellular myxozoan parasite (Tetracapsuloides bryosalmonae) through mark-recapture field sampling and the integration of RNA-sequencing with classical regression-based selection analysis. We show, based on fin transcriptomes of the host, that infection by the parasite and subsequent host survival is linked to upregulation of mitotic cell cycle process. We also detect a widespread signal of disruptive selection on transcripts linked to host immune defence, host-pathogen interactions, cellular repair and maintenance. Our results provide insights into how selection can be measured at the transcriptome level to dissect the molecular mechanisms of contemporary evolution driven by climate change and emerging anthropogenic threats. We anticipate that the approach described here will enable critical information on the molecular processes and targets of natural selection to be obtained in real time.

Automated summary

The study introduces a new analytical framework for quantifying ongoing natural selection at the transcriptome level in wild vertebrates. By integrating mark-recapture field sampling and RNA-sequencing with regression-based selection analysis, the study estimated selection on transcript abundance in wild salmonid fish affected by an extracellular parasite. The results reveal upregulation of mitotic cell cycle process in infected hosts and disruptive selection signals on transcripts related to host immune defense, host-pathogen interactions, cellular repair, and maintenance.