Abstract

Acclimation allowed by variation in gene or allele expression in natural populations is increasingly understood as a decisive mechanism, as much as adaptation, for species evolution. However, for small eukaryotic organisms, as species from zooplankton, classical methods face numerous challenges. Here, we propose the concept of allelic differential expression at the population‐scale (psADE) to investigate the variation in allele expression in natural populations. We developed a novel approach to detect psADE based on metagenomic and metatranscriptomic data from environmental samples. This approach was applied on the widespread marine copepod, Oithona similis, by combining samples collected during the Tara Oceans expedition (2009–2013) and de novo transcriptome assemblies. Among a total of 25,768 single nucleotide variants (SNVs) of O. similis, 572 (2.2%) were affected by psADE in at least one population (FDR < 0.05). The distribution of SNVs under psADE in different populations is significantly shaped by population genomic differentiation (Pearson r = 0.87, p = 5.6 × 10−30), supporting a partial genetic control of psADE. Moreover, a significant amount of SNVs (0.6%) were under both selection and psADE (p < .05), supporting the hypothesis that natural selection and psADE tends to impact common loci. Population‐scale allelic differential expression offers new insights into the gene regulation control in populations and its link with natural selection.

Highlights

  • Variation in gene expression within and between individuals or natural populations is an important mechanism for the acclimation of species (Fay & Wittkopp, 2008; Hutter, Saminadin-Peter, Stephan, & Parsch, 2008; Li, Liu, Kim, Min, & Zhang, 2010; Whitehead, 2012)

  • Marine species populations belonging to plankton face a large panel of physico-chemical changes in open ocean, (Guinder & Molinero, 2013; Pelejero, Calvo, & HoeghGuldberg, 2010) and gene expression variations have been observed in several studies (Lauritano, Procaccini, & Ianora, 2012; Salazar et al 2019)

  • We proposed to measure the population-scale allelic differential expression of genes. psADE depends on the difference between alleles abundance at the genomic and transcriptomic level

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Summary

| INTRODUCTION

Variation in gene expression within and between individuals or natural populations is an important mechanism for the acclimation of species (Fay & Wittkopp, 2008; Hutter, Saminadin-Peter, Stephan, & Parsch, 2008; Li, Liu, Kim, Min, & Zhang, 2010; Whitehead, 2012). An alternative approach could be to take advantage of the recent advances in metagenomic and metatranscriptomic sequencing of environmental samples, which offer a direct populational insight In this context, polymorphic sites of a single species have to be extracted, allowing to evaluate whether the population-scale relative expression of an allele deviates from its genomic frequency. Species belonging to the Oithona genus, are small crustaceans forming the most abundant metazoan on Earth (Gallienne, 2001; Humes, 1994; Kiørboe, 2011) This abundance, reflecting strong adaptive capacities to environmental fluctuations, together with large hypothetic effective population size (Peijnenburg & Goetze, 2013; Riginos, Crandall, Liggins, Bongaerts, & Treml, 2016; Madoui et al 2017; Arif et al 2018) make this species suitable for population genomics analyses. Variants of O. similis were extracted and the Allelic differential expression

| MATERIALS AND METHODS
| DISCUSSION
Findings
| CONCLUSION
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