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The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
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Papa, F. ; Windbichler, N. ; Waterhouse, R. M. ; Cagnetti, A. ; D'Amato, R. ; Persampieri, T. ; Lawniczak, M. K. N. ; Nolan, T. ; Papathanos, P. A. Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes. Genome research 2017, 27, 1536 - 1548. Publisher's VersionAbstract
Understanding how phenotypic differences between males and females arise from the sex-biased expression of nearly identical genomes can reveal important insights into the biology and evolution of a species. Among Anopheles mosquito species, these phenotypic differences include vectorial capacity, as it is only females that blood feed and thus transmit human malaria. Here, we use RNA-seq data from multiple tissues of four vector species spanning the Anopheles phylogeny to explore the genomic and evolutionary properties of sex-biased genes. We find that, in these mosquitoes, in contrast to what has been found in many other organisms, female-biased genes are more rapidly evolving in sequence, expression, and genic turnover than male-biased genes. Our results suggest that this atypical pattern may be due to the combination of sex-specific life history challenges encountered by females, such as blood feeding. Furthermore, female propensity to mate only once in nature in male swarms likely diminishes sexual selection of post-reproductive traits related to sperm competition among males. We also develop a comparative framework to systematically explore tissue- and sex-specific splicing to document its conservation throughout the genus and identify a set of candidate genes for future functional analyses of sex-specific isoform usage. Finally, our data reveal that the deficit of male-biased genes on the X Chromosomes in Anopheles is a conserved feature in this genus and can be directly attributed to chromosome-wide transcriptional regulation that de-masculinizes the X in male reproductive tissues.
Bernardini, F. ; Galizi, R. ; Wunderlich, M. ; Taxiarchi, C. ; Kranjc, N. ; Kyrou, K. ; Hammond, A. ; Nolan, T. ; Lawniczak, M. N. K. ; Papathanos, P. A. ; et al. Cross-Species Y Chromosome Function Between Malaria Vectors of the Species Complex. Genetics 2017, 207, 729-740.Abstract
Y chromosome function, structure and evolution is poorly understood in many species, including the genus of mosquitoes-an emerging model system for studying speciation that also represents the major vectors of malaria. While the Anopheline Y had previously been implicated in male mating behavior, recent data from the complex suggests that, apart from the putative primary sex-determiner, no other genes are conserved on the Y. Studying the functional basis of the evolutionary divergence of the Y chromosome in the gambiae complex is complicated by complete F1 male hybrid sterility. Here, we used an F1 × F0 crossing scheme to overcome a severe bottleneck of male hybrid incompatibilities that enabled us to experimentally purify a genetically labeled Y chromosome in an background. Whole genome sequencing (WGS) confirmed that the Y retained its original sequence content in the genomic background. In contrast to comparable experiments in , we find that the presence of a heterospecific Y chromosome has no significant effect on the expression of genes, and transcriptional differences can be explained almost exclusively as a direct consequence of transcripts arising from sequence elements present on the Y chromosome itself. We find that Y hybrids show no obvious fertility defects, and no substantial reduction in male competitiveness. Our results demonstrate that, despite their radically different structure, Y chromosomes of these two species of the gambiae complex that diverged an estimated 1.85 MYA function interchangeably, thus indicating that the Y chromosome does not harbor loci contributing to hybrid incompatibility. Therefore, Y chromosome gene flow between members of the gambiae complex is possible even at their current level of divergence. Importantly, this also suggests that malaria control interventions based on sex-distorting Y drive would be transferable, whether intentionally or contingent, between the major malaria vector species.
Coll, M. ; Wajnberg, E. Environmental Pest Management. In Environmental Pest Management; Environmental Pest Management; John Wiley & Sons, Ltd, 2017; pp. 405-417. Publisher's VersionAbstract
Summary For thousands of years, farmers have protected their crops by combating one pest at a time, using a single control method with very little consideration of the surrounding environment. In its early form, Integrated Pest Management (IPM) was intended to provide a more holistic approach to pest management than the ‘supervised control’ that was commonplace at the time. However, when public support later declined, agro-chemical companies were quick to step in and take on a major role in directing pest management back towards supervised control. To reduce yield losses to pests and produce more food in sustainable and environmentally compatible ways, major long-term governmental commitments are needed. We argue that governmental inputs acting to promote sustainable agricultural practices and nature conservation should have four main thrusts that are currently missing in most legislation: (1) establishing goal-oriented agro-environmental schemes, (2) externalizing the true costs of pesticide use, (3) strengthening the public extension service, and (4) soliciting goal-specific research.
Coll, M. ; Wajnberg, E. Environmental Pest Management. In Environmental Pest Management; Environmental Pest Management; John Wiley & Sons, Ltd, 2017; pp. 1-17. Publisher's VersionAbstract
Summary Increasing awareness and concerns regarding the adverse effects of pest management activities on human health and the environment have led researchers and, to a lesser extent non-governmental activists and policymakers, to seek ways to restrain harmful pest control practices. Conservation biologists, in their efforts to protect biodiversity, have begun to document the importance of the environment in pest management. At the same time, the Integrated Pest Management (IPM) approach, formulated more than 55 years ago, has for the most part failed to fulfil its mission developing effective, safe and sustainable plant protection systems. To this end, a new pest management paradigm is needed: a top-down, system-centric approach should replace the historical bottom-up, pest-centric viewpoint. This change is particularly important if we are to harness pest control activities to a global effort to increase food security and environmental protection.
Coll, M. ; Wajnberg, E. Environmental Pest Management: Challenges for Agronomists, Ecologists, Economists and Policymakers; John Wiley & Sons, Ltd, 2017. Publisher's VersionAbstract

A wide-ranging, interdisciplinary exploration of key topics that interrelate pest management, public health and the environment

This book takes a unique, multidimensional approach to addressing the complex issues surrounding pest management activities and their impacts on the environment and human health, and environmental effects on plant protection practices.

It features contributions by a distinguished group of authors from ten countries, representing an array of disciplines. They include plant protection scientists and officers, economists, agronomists, ecologists, environmental and public health scientists and government policymakers. Over the course of eighteen chapters, those experts share their insights into and analyses of an array of issues of vital concern to everyone with a professional interest in this important subject.

The adverse effects of pest control have become a subject of great concern worldwide, and researchers and enlightened policymakers have at last begun to appreciate the impact of environmental factors on our ability to manage pest populations. Moreover, while issues such as pesticide toxicity have dominated the global conversation about pest management, economic and societal considerations have been largely neglected. Environmental Pest Management: Challenges for Agronomists, Ecologists, Economists and Policymakers is the first work to provide in-depth coverage of all of these pressing issues between the covers of one book.

• Offers a unique multi-dimensional perspective on the complex issues surrounding pest management activities and their effect on the environment and human health

• Addresses growing concerns about specific pest management strategies, including the use of transgenic crops and biological controls

• Analyses the influence of global processes, such as climate change, biological invasions and shifts in consumer demand, and ecosystem services and disservices on pest suppression efforts

• Explores public health concerns regarding biodiversity, pesticide use and food safety

• Identifies key economic drivers of pest suppression research, strategies and technologies

• Proposes new regulatory approaches to create sustainable and viable crop protection systems in the framework of agroenvironmental schemes

Offering a timely and comprehensively-unique treatment of pest management and its environmental impacts in a single, interdisciplinary volume, this book is a valuable resource for scientists in an array of disciplines, as well as government officials and policymakers. Also, teachers of undergraduate and graduate level courses in a variety of fields are sure to find it a highly useful teaching resource.

Schuldiner-harpaz, T. ; Coll, M. Estimating the effect of plant-provided food supplements on pest consumption by omnivorous predators: lessons from two coccinellid beetles. Pest Manag Sci 2017, 73, 976-983.Abstract
BACKGROUND: Plant-provided food supplements can influence biological pest control by omnivorous predators in two counteracting ways: they can (i) enhance predator populations, but (ii) reduce pest consumption by individual predators. Yet the majority of studies address only one of these aspects. Here, we first tested the influence of canola (Brassica napus L.) pollen supplements on the life history of two ladybeetle species: Hoppodamia variegata (Goeze) and Coccinella septempunctata (L.). We then developed a theoretical model to simulate total pest consumption in the presence and absence of pollen supplements. RESULTS: Supplementing a prey diet with canola pollen increased H. variegata larval survival from 50 to 82%, and C. septempunctata female oviposition by 1.6-fold. Model simulations revealed a greater benefit of pollen supplements when relying on C. septempunctata for pest suppression than on H. variegata. CONCLUSION: For these two predators, the tested pollen serves as an essential supplement to a diet of prey. However, the benefit of a mixed prey-pollen diet was not always sufficient to overcome individual decrease in pest consumption. Taken together, our study highlights the importance of addressing both positive and negative roles of plant-provided food supplements in considering the outcome for biological control efforts that rely on omnivorous predators. © 2016 Society of Chemical Industry.
Zarchin, S. ; Dag, A. ; Salomon, M. ; Hendriksma, H. P. ; Shafir, S. Honey bees dance faster for pollen that complements colony essential fatty acid deficiency. Behavioral Ecology and Sociobiology 2017, 71, 172. Publisher's VersionAbstract
Honey bee colonies require adequate pollen for maintenance and growth. Pollens vary in nutritional value, and a balanced diet is achieved by mixing pollens with complementary essential nutrients. We tested subjective evaluation of pollens by foragers in colonies deprived of one of two essential fatty acids (eFAs), alpha-linolenic acid (omega-3) or linoleic acid (omega-6). We used four pollens, two rich in omega-3 and two rich in omega-6. A colony in an observation hive was allowed to forage for 2–5 days on a single pollen source. The following day, we repeatedly presented one of three pollens: the same pollen that the bees had been collecting the previous days, a novel pollen that was similarly deficient in omega-3 or omega-6, and a novel pollen that complemented their eFA deficiency. We measured the rate of waggle dances, which reflects on the strength of recruitment effort, of foragers returning to the observation hive from each of the pollens. Dance rates did not differ between the four pollens, but they were the highest to the ``complementary'' pollen and the lowest to the ``same'' pollen. Furthermore, this effect was greater for pollen combinations with greater eFA disparity between the same and the complementary pollens. Our findings support the ability of bees to balance colony eFA intake. Conditioning of the proboscis extension response (PER) tests showed that pollen foragers discriminated well between the four pollen odors, but the mechanisms by which bees assess pollen eFA composition remain to be elucidated. Differential dancing would recruit foragers to pollens that balance colony nutritional needs.
Yuval, B. Symbiosis: Gut Bacteria Manipulate Host Behaviour. Current Biology 2017, 27, R746 - R747. Publisher's VersionAbstract
Summary Bacteria resident in the gut of Drosophila modify the fly’s innate chemosensory responses to nutritional stimuli. In effect, the gut microbiome compels the host to forage on food patches that favour particular assemblages of bacteria.
Sapir, G. ; Baras, Z. ; Azmon, G. ; Goldway, M. ; Shafir, S. ; Allouche, A. ; STERN, E. ; Stern, R. A. Synergistic effects between bumblebees and honey bees in apple orchards increase cross pollination, seed number and fruit size. Scientia Horticulturae 2017, 219, 107 - 117. Publisher's VersionAbstract
Most apple cultivars are self-sterile and completely dependent on cross-pollination from a different cultivar in order to set fruit. Various insects may be pollinators, but the main one is the honey bee [HB] (Apis mellifera). However, despite the advantages of the honey bee as pollinator of many plants, it is a relatively inefficient pollinator of apple flowers. The main reason for this is the tendency of HBs to visit the apple flower from the side (sideworker), thus “stealing” nectar without touching the flower’s reproductive organs – stamens and stigma. In contrast, a bee that visits the flower from the top (topworker) contacts the flower’s reproductive organs, which results in better pollination. Due to the low pollination efficiency, few seeds are formed, and often the resulting fruit is too small to be of commercial value. Experiments conducted in Israel over the last few years have shown for the first time that adding bumblebees [BB] (Bombus terrestris) into pear orchards improved cross-pollination, thus increasing the number of seeds and subsequently fruit size. The goal of the present work was to test the hypothesis that adding BBs to apple orchards may improve cross-pollination. We found that adding BBs to the HBs in the apple orchard improved pollination in all tested cultivars, especially in ‘Gala’, which naturally suffers from relatively few seeds in the fruit. It appears that the addition of BBs did not only increase the number of pollinating insects in the orchard that could perform cross-pollination, including in the cool mornings and in adverse weather conditions, but that it also changed HB foraging behavior, which resulted in improved cross-pollination and increased efficiency, and subsequently more seeds and larger fruit. The improved pollination was due to the greater mobility of HBs between rows of pollinated cultivar and pollenizer, and to the greater proportion of topworkers, which are more efficient pollinators.
Santos-Garcia, D. ; Silva, F. J. ; Morin, S. ; Dettner, K. ; Kuechler, S. M. The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution. Genome Biology and Evolution 2017, 9 2893 - 2910. Publisher's VersionAbstract
Hemipteran insects are well-known in their ability to establish symbiotic relationships with bacteria. Among them, heteropteran insects present an array of symbiotic systems, ranging from the most common gut crypt symbiosis to the more restricted bacteriome-associated endosymbiosis, which have only been detected in members of the superfamily Lygaeoidea and the family Cimicidae so far. Genomic data of heteropteran endosymbionts are scarce and have merely been analyzed from the Wolbachia endosymbiont in bed bug and a few gut crypt-associated symbionts in pentatomoid bugs. In this study, we present the first detailed genomic analysis of a bacteriome-associated endosymbiont of a phytophagous heteropteran, present in the seed bug Henestaris halophilus (Hemiptera: Heteroptera: Lygaeoidea). Using phylogenomics and genomics approaches, we have assigned the newly characterized endosymbiont to the Sodalis genus, named as Candidatus Sodalis baculum sp. nov. strain kilmister. In addition, our findings support the reunification of the Sodalis genus, currently divided into six different genera. We have also conducted comparative analyses between 15 Sodalis species that present different genome sizes and symbiotic relationships. These analyses suggest that Ca. Sodalis baculum is a mutualistic endosymbiont capable of supplying the amino acids tyrosine, lysine, and some cofactors to its host. It has a small genome with pseudogenes but no mobile elements, which indicates middle-stage reductive evolution. Most of the genes in Ca. Sodalis baculum are likely to be evolving under purifying selection with several signals pointing to the retention of the lysine/tyrosine biosynthetic pathways compared with other Sodalis.
Sparks, J. T. ; Bohbot, J. D. ; Ristić, M. ; Mišić, D. ; Skorić, M. ; Mattoo, A. ; Dickens, J. C. Chemosensory Responses to the Repellent Nepeta Essential Oil and Its Major Component Nepetalactone by Aedes aegypti (Diptera: Culicidae), a Vector of Zika Virus. Journal of Medical Entomology 2017, 54, 957 - 963. Publisher's VersionAbstract
Nepeta essential oil (Neo; catnip) and its major component, nepetalactone, have long been known to repel insects including mosquitoes. However, the neural mechanisms through which these repellents are detected by mosquitoes, including the yellow fever mosquito Aedes aegypti (L.), an important vector of Zika virus, were poorly understood. Here we show that Neo volatiles activate olfactory receptor neurons within the basiconic sensilla on the maxillary palps of female Ae. aegypti. A gustatory receptor neuron sensitive to the feeding deterrent quinine and housed within sensilla on the labella of females was activated by both Neo and nepetalactone. Activity of a second gustatory receptor neuron sensitive to the feeding stimulant sucrose was suppressed by both repellents. Our results provide neural pathways for the reported spatial repellency and feeding deterrence of these repellents. A better understanding of the neural input through which female mosquitoes make decisions to feed will facilitate design of new repellents and management strategies involving their use.
Schuldiner-harpaz, T. ; Coll, M. Effect of Diet History on Prey and Pollen Food Choice by Two Lady Beetle Species. Journal of Insect Behavior 2017, 30, 432-438. Publisher's VersionAbstract
Mixed diets of prey and plant-provided foods, such as pollen, have been shown to benefit a wide range of arthropods. However, diet shifting between these two very different food sources remains poorly understood. We hypothesized that previous diet should influence subsequent time allocation between prey and plant food types; to reach a balanced diet, consumers are expected to allocate more time to resources previously lacking in their diet. We tested this hypothesis by observing the foraging choices of larvae of two omnivorous coccinellid species: Coccinella septempunctata L. and Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae), following a diet history of prey, pollen or a mixed diet of both food types. Results showed an asymmetrical tendency of C. septempunctata larvae to complement their previous diet with unfamiliar food: larvae allocated more time to pollen feeding, but not to prey, when each of the foods was previously absent from their diet. Study results have important implications for the use of plant-provided food supplements to enhance biological control by these omnivorous consumers.
Ben-Yosef, M. ; Zaada, D. S. Y. ; Dudaniec, R. Y. ; Pasternak, Z. ; Jurkevitch, E. ; Smith, R. J. ; Causton, C. E. ; Lincango, M. P. ; Tobe, S. S. ; Mitchell, J. G. ; et al. Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands. Mol Ecol 2017, 26, 4644-4656.Abstract
The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host-parasite co-evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host-related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.
Pavlidi, N. ; Gioti, A. ; Wybouw, N. ; Dermauw, W. ; Ben-Yosef, M. ; Yuval, B. ; Jurkevitch, E. ; Kampouraki, A. ; Van Leeuwen, T. ; Vontas, J. Transcriptomic responses of the olive fruit fly Bactrocera oleae and its symbiont Candidatus Erwinia dacicola to olive feeding. Sci Rep 2017, 7 42633.Abstract
The olive fruit fly, Bactrocera oleae, is the most destructive pest of olive orchards worldwide. The monophagous larva has the unique capability of feeding on olive mesocarp, coping with high levels of phenolic compounds and utilizing non-hydrolyzed proteins present, particularly in the unripe, green olives. On the molecular level, the interaction between B. oleae and olives has not been investigated as yet. Nevertheless, it has been associated with the gut obligate symbiotic bacterium Candidatus Erwinia dacicola. Here, we used a B.oleae microarray to analyze the gene expression of larvae during their development in artificial diet, unripe (green) and ripe (black) olives. The expression profiles of Ca. E. dacicola were analyzed in parallel, using the Illumina platform. Several genes were found overexpressed in the olive fly larvae when feeding in green olives. Among these, a number of genes encoding detoxification and digestive enzymes, indicating a potential association with the ability of B. oleae to cope with green olives. In addition, a number of biological processes seem to be activated in Ca. E. dacicola during the development of larvae in olives, with the most notable being the activation of amino-acid metabolism.