Abstract

Chromosome rearrangements are arguably the most dramatic type of mutations, often leading to rapid evolution and speciation. However, chromosome dynamics have only been studied at the sequence level in a small number of model systems. In insects, Diptera and Lepidoptera have conserved genome structure at the scale of whole chromosomes or chromosome arms. Whether this reflects the diversity of insect genome evolution is questionable given that many species exhibit rapid karyotype evolution. Here, we investigate chromosome evolution in aphids—an important group of hemipteran plant pests—using newly generated chromosome-scale genome assemblies of the green peach aphid (Myzus persicae) and the pea aphid (Acyrthosiphon pisum), and a previously published assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganization over the last 30 My, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (Myzus persicae and Acyrthosiphon pisum) and Aphidini (Rhopalosiphum maidis). In contrast, gene content of the aphid sex (X) chromosome remained unchanged despite rapid sequence evolution, low gene expression, and high transposable element load. To test whether rapid evolution of genome structure is a hallmark of Hemiptera, we compared our aphid assemblies with chromosome-scale assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny. The exceptional rate of structural evolution of aphid autosomes renders them an important emerging model system for studying the role of large-scale genome rearrangements in evolution.

Highlights

  • Mutation generates genomic novelty upon which natural selection and genetic drift can act to drive evolutionary change (Charlesworth 2009; Lynch et al 2016; Charlesworth and Charlesworth 2017; Good et al 2017)

  • For M. persicae, we report the first chromosome-scale genome assembly of this species with 97% of the assembled content contained in six scaffolds corresponding to the haploid chromosome number of this species (Blackman 1980)

  • Our M. persicae and A. pisum genome assemblies are accurate at the gene-level, containing 94% and 98% of conserved Arthropoda benchmarking universal single-copy orthologs (BUSCO) genes (n=1,066) as complete, single copies, respectively (Supplementary Figure 3)

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Summary

Introduction

Mutation generates genomic novelty upon which natural selection and genetic drift can act to drive evolutionary change (Charlesworth 2009; Lynch et al 2016; Charlesworth and Charlesworth 2017; Good et al 2017). Chromosomes may undergo extensive rearrangement via inversions, translocations, fusions and fissions (Eichler and Sankoff 2003). These macromutations can have dramatic consequences by altering gene regulation (Farré et al 2019; Stewart and Rogers 2019) and modifying local recombination rates (Farré et al 2013; Martin et al 2019), and they are implicated in key evolutionary processes such as adaptation and speciation (Rieseberg 2001; Kirkpatrick and Barton 2006; Chang et al 2013; Guerrero and Kirkpatrick 2014; Fuller et al 2019; Wellband et al 2019). In insects, these studies have been restricted to a few holometabolous groups, such as Diptera (mainly Drosophila and mosquitoes) and Lepidoptera (butterflies) that have been the focus of concerted genome sequencing efforts

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