Abstract

Ecology of insects is as wide as their diversity, which reflects their high capacity of adaptation in most of the environments of our planet. Aphids, with over 4,000 species, have developed a series of adaptations including a high phenotypic plasticity and the ability to feed on the phloem sap of plants, which is enriched in sugars derived from photosynthesis. Recent analyses of aphid genomes have indicated a high level of shared ancestral gene duplications that might represent a basis for genetic innovation and broad adaptations. In addition, there are a large number of recent, species-specific gene duplications whose role in adaptation remains poorly understood. Here, we tested whether duplicates specific to the pea aphid Acyrthosiphon pisum are related to genomic innovation by combining comparative genomics, transcriptomics, and chromatin accessibility analyses. Consistent with large levels of neofunctionalization, we found that most of the recent pairs of gene duplicates evolved asymmetrically, showing divergent patterns of positive selection and gene expression. Genes under selection involved a plethora of biological functions, suggesting that neofunctionalization and tissue specificity, among other evolutionary mechanisms, have orchestrated the evolution of recent paralogs in the pea aphid and may have facilitated host–symbiont cooperation. Our comprehensive phylogenomics analysis allowed us to tackle the history of duplicated genes to pave the road toward understanding the role of gene duplication in ecological adaptation.

Highlights

  • Aphids are insect pests belonging to the order Hemiptera, which diverged some 280–250 Ma

  • We show that 1) a large proportion of gene duplications are under positive selection in A. pisum and affect a large number of biological functions, 2) asymmetrical rates of young paralogs coupled to positive selection suggest that neofunctionalization is a main force reshaping the pea aphid genome, 3) a third of young duplicates show divergent tissue expression patterns, consistent in some cases with subfunctionalization by tissue specialization and others with neofunctionalization through gain of gene expression, and 4) chromatin accessibility of the transcription start site (TSS) can change between genes in duplicated gene pairs, it cannot directly explain their transcriptional state in A. pisum

  • Young Paralogs in A. pisum Are under Neofunctionalization and Involve Diverse Biological Functions We built a phylome for A. pisum in the context of hemipteran evolution, including five additional aphid species and three basal Sternorrhyncha species

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Summary

Introduction

Aphids are insect pests belonging to the order Hemiptera, which diverged some 280–250 Ma. Several aphid genomes are publically available, and all show a high level of gene duplication and expansions (International Aphid Genomics Consortium 2010; Mathers et al 2017; Li et al 2019). Some of these duplications are shared between aphid species, but most of them are lineage specific (International Aphid Genomics Consortium 2010). Whether or not duplicated or expanded gene families are in relation with the above-mentioned or other functional innovations enabling adaptive evolution in aphids is still largely unknown

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