Molecular ecology of insect pests of agricultural importance: the case of aphids

1. Ongoing environmental change is predicted to have a strong impact on biodiversity. Studies have already noted a range shift in many species as they track their favoured environments. A key challenge entomologists are facing is to understand how insect pest species are responding to this rapid environmental change, and molecular ecology has a central role to play in this task. In the present paper, I argue that molecular ecology has much relevance in relation to the monitoring of insect pests of agricultural importance, with a focus on aphids. 2. First, I examine how the combination of phylogeography and species distribution modelling can be a powerful approach to understanding species responses to climate change and to forecasting future distributions. Despite such a joint approach being increasingly used to understand these questions (e.g. in conservation biology), there are still very few studies that concern pest species of agricultural importance. 3. I then discuss how the use of samples from natural history collections represent an opportunity to directly observe the evolution of species, enhancing our knowledge of the evolutionary processes occurring at ecological time scales. I introduce the Rothamsted Insect Survey (RIS) sample archive and the central role it plays in the studies of pest species of agricultural importance. 4. Lastly, I assess how the advances in DNA sequencing technologies have allowed us to investigate genetic variation at the genome-wide level. Thus, they provide us with the opportunity of studying a variety of questions about the dynamics of pest insects that were previously impossible as well as unmanageable

Contrasting population structure and demographic history of cereal aphids in different environmental and agricultural landscapes

Genetic diversity of populations has important ecological and evolutionary consequences, whose understanding is fundamental to improve the sustainability of agricultural production. Studies of how differences in agricultural management and environment influence the population structure of insect pests are central to predict outbreaks and optimise control programmes. Here, we have studied the population genetic diversity and evolution of Sitobion avenae and Sitobion miscanthi, which are among the most relevant aphid pests of cereals across Europe and Asia, respectively. We have used genotyping by sequencing (GBS) to identify genome-wide single nucleotide polymorphisms (SNPs) to infer the geographic structure and migration patterns. In the present study, we show that the population structure in present day populations are different from that described in previous studies, which suggests that they have evolved recently possibly as a response to human-induced changes in agriculture. This study shows that S. avenae in England is predominantly parthenogenetic and there has been a demographic and spatial expansion of a single genetic cluster, which could correspond with the insecticide-resistance superclone identified in previous studies. Conversely, in China, S. miscanthi populations are mostly cyclical parthenogenetic, with one sexual stage in autumn to produce overwintering eggs, and there are six genetically differentiated subpopulations and high genetic differentiation between geographic locations, which suggests that further taxonomical research is needed. Unlike S. avenae in England, there is no evidence for insecticide resistance and there is no predominance of a single lineage in S. miscanthi in China

Genome assembly and transcriptomic analysis to elucidate the ability of Nasonovia ribisnigri to break host plant resistance

Aphid genomic resources enable the study of complex life history traits and provide information on vector biology, host adaption and speciation. The currant–lettuce aphid (Nasonovia ribisnigri (Hemiptera: Aphididae) (Mosley)) is a cosmopolitan pest of outdoor lettuce (Lactuca sativa (Asterales: Asteraceae) (Linnaeus)). Until recently, the use of resistant cultivars was an effective method for managing N. ribisnigri. A resistant cultivar containing a single gene (Nr‐locus), introduced in the 1980s, conferred complete resistance to feeding. Overreliance of this Nr‐locus in lettuce resulted in N. ribisnigri's ability to break resistance mechanism, with first reports during 2003. Our work attempts to understand which candidate gene(s) are associated with this resistance‐breaking mechanism. We present two de novo draft assembles for N. ribisnigri genomes, corresponding to both avirulent (Nr‐locus susceptible) and virulent (Nr‐locus resistant) biotypes. Changes in gene expression of the two N. ribisnigri biotypes were investigated using transcriptomic analyses of RNA‐sequencing (RNA‐seq) data to understand the potential mechanisms of resistance to the Nr‐locus in lettuce. The draft genome assemblies were 94.2% and 91.4% complete for the avirulent and virulent biotypes, respectively. Out of the 18,872 differentially expressed genes, a single gene/locus was identified in N. ribisnigri that was shared between two resistant‐breaking biotypes. This locus was further explored and validated in Real‐Time Quantitative Reverse Transcription PCR (qRT‐PCR) experiments and has predicted localisations in both the cytoplasm and nucleus. This is the first study to provide evidence that a single gene/locus is likely responsible for the ability of N. ribisnigri to overcome the Nr‐locus resistance in the lettuce host

Population genetic structure and predominance of cyclical parthenogenesis in the bird cherry–oat aphid Rhopalosiphum padi in England

Genetic diversity is determinant for pest species' success and vector competence. Understanding the ecological and evolutionary processes that determine the genetic diversity is fundamental to help identify the spatial scale at which pest populations are best managed. In the present study, we present the first comprehensive analysis of the genetic diversity and evolution of Rhopalosiphum padi, a major pest of cereals and a main vector of the barley yellow dwarf virus (BYDV), in England. We have used a genotyping by sequencing approach to study whether i) there is any underlying population genetic structure at a national and regional scale in this pest that can disperse long distances; ii) the populations evolve as a response to environmental change and selective pressures, and; iii) the populations comprise anholocyclic lineages. Individual R. padi were collected using the Rothamsted Insect Survey's suction‐trap network at several sites across England between 2004 and 2016 as part of the RIS long‐term nationwide surveillance. Results identified two genetic clusters in England that mostly corresponded to a North – South division, although gene flow is ongoing between the two subpopulations. These genetic clusters do not correspond to different life cycles types, and cyclical parthenogenesis is predominant in England. Results also show that there is dispersal with gene flow across England, although there is a reduction between the northern and southern sites with the Southwestern population being the most genetically differentiated. There is no evidence for isolation‐by‐distance and other factors like primary host distribution, uncommon in the south and absent in the southwest, could influence the dispersal patterns. Finally, results also show no evidence for the evolution of the R. padi population, and it is demographically stable despite the ongoing environmental change. These results are discussed in view of their relevance to pest management and the transmission of BYDV

The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for Bluetongue virus

Background The new genomic technologies have provided novel insights into the genetics of interactions between vectors, viruses and hosts, which are leading to advances in the control of arboviruses of medical importance. However, the development of tools and resources available for vectors of non-zoonotic arboviruses remains neglected. Biting midges of the genus Culicoides transmit some of the most important arboviruses of wildlife and livestock worldwide, with a global impact on economic productivity, health and welfare. The absence of a suitable reference genome has hindered genomic analyses to date in this important genus of vectors. In the present study, the genome of Culicoides sonorensis, a vector of bluetongue virus (BTV) in the USA, has been sequenced to provide the first reference genome for these vectors. In this study, we also report the use of the reference genome to perform initial transcriptomic analyses of vector competence for BTV. Results Our analyses reveal that the genome is 189 Mb, assembled in 7974 scaffolds. Its annotation using the transcriptomic data generated in this study and in a previous study has identified 15,612 genes. Gene expression analyses of C. sonorensis females infected with BTV performed in this study revealed 165 genes that were differentially expressed between vector competent and refractory females. Two candidate genes, glutathione S-transferase (gst) and the antiviral helicase ski2, previously recognized as involved in vector competence for BTV in C. sonorensis (gst) and repressing dsRNA virus propagation (ski2), were confirmed in this study. Conclusions The reference genome of C. sonorensis has enabled preliminary analyses of the gene expression profiles of vector competent and refractory individuals. The genome and transcriptomes generated in this study provide suitable tools for future research on arbovirus transmission. These provide a valuable resource for these vector lineage, which diverged from other major Dipteran vector families over 200 million years ago. The genome will be a valuable source of comparative data for other important Dipteran vector families including mosquitoes (Culicidae) and sandflies (Psychodidae), and together with the transcriptomic data can yield potential targets for transgenic modification in vector control and functional studies

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

This work was financially support by a Marie Curie Initial Training Network grant, “Understanding the evolutionary origin of biological diversity” (ITN-2008–213780 SPECIATION), grants from the Academy of Finland to A.H. (project 132619) and M.K. (projects 268214 and 272927), a grant from NERC, UK to M.G.R. (grant NE/J020818/1), and NERC, UK PhD studentship to D.J.P. (NE/I528634/1).For many organisms the ability to cold acclimate with the onset of seasonal cold has major implications for their fitness. In insects, where this ability is widespread, the physiological changes associated with increased cold tolerance have been well studied. Despite this, little work has been done to trace changes in gene expression during cold acclimation that lead to an increase in cold tolerance. We used an RNA-Seq approach to investigate this in two species of the Drosophila virilis group. We found that the majority of genes that are differentially expressed during cold acclimation differ between the two species. Despite this, the biological processes associated with the differentially expressed genes were broadly similar in the two species. These included: metabolism, cell membrane composition, and circadian rhythms, which are largely consistent with previous work on cold acclimation/cold tolerance. In addition, we also found evidence of the involvement of the rhodopsin pathway in cold acclimation, a pathway that has been recently linked to thermotaxis. Interestingly, we found no evidence of differential expression of stress genes implying that long-term cold acclimation and short-term stress response may have a different physiological basis.PostprintPeer reviewe