BackgroundThe prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Insect herbivores are no exception and the majority have evolved to colonise a small number of closely related host species. Remarkably, the green peach aphid, Myzus persicae, colonises plant species across 40 families and single M. persicae clonal lineages can colonise distantly related plants. This remarkable ability makes M. persicae a highly destructive pest of many important crop species.ResultsTo investigate the exceptional phenotypic plasticity of M. persicae, we sequenced the M. persicae genome and assessed how one clonal lineage responds to host plant species of different families. We show that genetically identical individuals are able to colonise distantly related host species through the differential regulation of genes belonging to aphid-expanded gene families. Multigene clusters collectively upregulate in single aphids within two days upon host switch. Furthermore, we demonstrate the functional significance of this rapid transcriptional change using RNA interference (RNAi)-mediated knock-down of genes belonging to the cathepsin B gene family. Knock-down of cathepsin B genes reduced aphid fitness, but only on the host that induced upregulation of these genes.ConclusionsPrevious research has focused on the role of genetic adaptation of parasites to their hosts. Here we show that the generalist aphid pest M. persicae is able to colonise diverse host plant species in the absence of genetic specialisation. This is achieved through rapid transcriptional plasticity of genes that have duplicated during aphid evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1145-3) contains supplementary material, which is available to authorized users.

statistics of 25 human-infective Cryptosporidium spp. genome projects including 23 whole genome sequences (WGS). * Included in whole genome comparative genomics ‡ Included in whole genome comparative genomics and recombination analysis # Used only for read mapping onto Iowa II in Figure 3b

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The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host–plant associations, uncovering the widespread co‐option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.

Large-scale 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 (flies and mosquitoes) and Lepidoptera (butterflies and moths) have high levels of chromosome conservation. Whether this truly 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 chromosome-scale assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganisation over the last 30 million years, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (M. persicae and A. pisum) and Aphidini (R. 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 to chromosome-level assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny and we detect only two chromosome fusion or fission events. 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.

Aphids present an ideal system to study epigenetics as they can produce diverse, but genetically identical, morphs in response to environmental stimuli. Here, using whole genome bisulphite sequencing and transcriptome sequencing of the green peach aphid (Myzus persicae), we present the first detailed analysis of cytosine methylation in an aphid and investigate differences in the methylation and transcriptional landscapes of male and asexual female morphs. We find that methylation primarily occurs in a CG dinucleotide (CpG) context and that exons are highly enriched for methylated CpGs, particularly at the 3' end of genes. Methylation is positively associated with gene expression, and methylated genes are more stably expressed than un-methylated genes. Male and asexual female morphs have distinct methylation profiles. Strikingly, these profiles are divergent between the sex chromosome and the autosomes; autosomal genes are hypo-methylated in males compared to asexual females, whereas genes belonging to the sex chromosome, which is haploid in males, are hyper-methylated. Overall, we find correlated changes in methylation and gene expression between males and asexual females, and this correlation is particularly strong for genes located on the sex chromosome. Our results suggest that differential methylation of sexbiased genes plays a role in M. persicae sexual differentiation.

‘Living fossils’, a phrase first coined by Darwin, are defined as species with limited recent diversification and high morphological stasis over long periods of evolutionary time. Morphological stasis, however, can potentially lead to diversification rates being underestimated. Notostraca, or tadpole shrimps, is an ancient, globally distributed order of branchiopod crustaceans regarded as ‘living fossils’ because their rich fossil record dates back to the early Devonian and their morphology is highly conserved. Recent phylogenetic reconstructions have shown a strong biogeographic signal, suggesting diversification due to continental breakup, and widespread cryptic speciation. However, morphological conservatism makes it difficult to place fossil taxa in a phylogenetic context. Here we reveal for the first time the timing and tempo of tadpole shrimp diversification by inferring a robust multilocus phylogeny of Branchiopoda and applying Bayesian divergence dating techniques using reliable fossil calibrations external to Notostraca. Our results suggest at least two bouts of global radiation in Notostraca, one of them recent, so questioning the validity of the ‘living fossils’ concept in groups where cryptic speciation is widespread.

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 reorganisation over the last 30 million years, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (M. persicae and A. pisum) and Aphidini (R. 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 to 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.