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

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

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

Onchocerciasis transmission in Ghana: Persistence under different control strategies and the role of the simuliid vectors

Background: The World Health Organization (WHO) aims at eliminating onchocerciasis by 2020 in selected African countries. Current control focuses on community-directed treatment with ivermectin (CDTI). In Ghana, persistent transmission has been reported despite long-term control. We present spatial and temporal patterns of onchocerciasis transmission in relation to ivermectin treatment history. Methodology/Principal Findings: Host-seeking and ovipositing blackflies were collected from seven villages in four regions of Ghana with 3–24 years of CDTI at the time of sampling. A total of 16,443 flies was analysed for infection; 5,812 (35.3%) were dissected for parity (26.9% parous). Heads and thoraces of 12,196 flies were dissected for Onchocerca spp. and DNA from 11,122 abdomens was amplified using Onchocerca primers. A total of 463 larvae (0.03 larvae/fly) from 97 (0.6%) infected and 62 (0.4%) infective flies was recorded; 258 abdomens (2.3%) were positive for Onchocerca DNA. Infections (all were O. volvulus) were more likely to be detected in ovipositing flies. Transmission occurred, mostly in the wet season, at Gyankobaa and Bosomase, with transmission potentials of, respectively, 86 and 422 L3/person/month after 3 and 6 years of CDTI. The numbers of L3/1,000 parous flies at these villages were over 100times the WHO threshold of one L3/1,000 for transmission control. Vector species influenced transmission parameters. At Asubende, the number of L3/1,000 ovipositing flies (1.4, 95% CI = 0–4) also just exceeded the threshold despite extensive vector control and 24 years of ivermectin distribution, but there were no infective larvae in host-seeking flies. Conclusions/Significance: Despite repeated ivermectin treatment, evidence of O. volvulus transmission was documented in all seven villages and above the WHO threshold in two. Vector species influences transmission through biting and parous rates and vector competence, and should be included in transmission models. Oviposition traps could augment vector collector methods for monitoring and surveillance

Cold adaptation drives population genomic divergence in the ecological specialist, Drosophila montana

Funding: UK Natural Environment Research Council (Grant Number(s): NE/L501852/1, NE/P000592/1); Academy of Finland (GrantNumber(s): 267244, 268214, 322980), Ella ja Georg Ehrnroothin Säätiö.Detecting signatures of ecological adaptation in comparative genomics is challenging, but analysing population samples with characterised geographic distributions, such as clinal variation, can help identify genes showing covariation with important ecological variation. Here, we analysed patterns of geographic variation in the cold-adapted species Drosophila montana across phenotypes, genotypes and environmental conditions and tested for signatures of cold adaptation in population genomic divergence. We first derived the climatic variables associated with the geographic distribution of 24 populations across two continents to trace the scale of environmental variation experienced by the species, and measured variation in the cold tolerance of the flies of six populations from different geographic contexts. We then performed pooled whole genome sequencing of these six populations, and used Bayesian methods to identify SNPs where genetic differentiation is associated with both climatic variables and the population phenotypic measurements, while controlling for effects of demography and population structure. The top candidate SNPs were enriched on the X and fourth chromosomes, and they also lay near genes implicated in other studies of cold tolerance and population divergence in this species and its close relatives. We conclude that ecological adaptation has contributed to the divergence of D. montana populations throughout the genome and in particular on the X and fourth chromosomes, which also showed highest interpopulation FST. This study demonstrates that ecological selection can drive genomic divergence at different scales, from candidate genes to chromosome-wide effects.Publisher PDFPeer reviewe

Data from: Niche evolution and thermal adaptation in the temperate species Drosophila americana

The study of ecological niche evolution is fundamental for understanding how the environment influences species’ geographical distributions and their adaptation to divergent environments. Here we present a study of the ecological niche, demographic history and thermal performance (locomotor activity, developmental time and fertility/viability) of the temperate species Drosophila americana and its two chromosomal forms. Temperature is the environmental factor that contributes most to the species’ and chromosomal forms’ ecological niches, although precipitation is also important in the model of the southern populations. The past distribution model of the species predicts a drastic reduction in the suitable area for the distribution of the species during the Last Glacial Maximum (LGM), suggesting a strong bottleneck. However, DNA analyses did not detect a bottleneck signature during the LGM. These contrasting results could indicate that D. americana niche preference evolves with environmental change and, thus, there is no evidence to support niche conservatism in this species. Thermal performance experiments show no difference in the locomotor activity across a temperature range of 15 to 38oC between flies from the north and the south of its distribution. However, we found significant differences in developmental time and fertility/viability between the two chromosomal forms at the model’s optimal temperatures for the two forms. However, results do not indicate that they perform better for the traits studied here in their respective optimal niche temperatures. This suggests that behaviour plays an important role in thermoregulation, supporting the capacity of this species to adapt to different climatic conditions across its latitudinal distribution