TY - JOUR A1 - Wolf, S. A1 - McMahon, Dino Peter A1 - Lim, K.S. A1 - Pull, C.D. A1 - Clark, S.J. A1 - Paxton, R.J. A1 - Osborne, J.L. T1 - So near and yet so far: harmonic radar reveals reduced homing ability of Nosema infected honeybees N2 - Pathogens may gain a fitness advantage through manipulation of the behaviour of their hosts. Likewise, host behavioural changes can be a defence mechanism, counteracting the impact of pathogens on host fitness. We apply harmonic radar technology to characterize the impact of an emerging pathogen - Nosema ceranae (Microsporidia) - on honeybee (Apis mellifera) flight and orientation performance in the field. Honeybees are the most important commercial pollinators. Emerging diseases have been proposed to play a prominent role in colony decline, partly through sub-lethal behavioural manipulation of their hosts. We found that homing success was significantly reduced in diseased (65.8%) versus healthy foragers (92.5%). Although lost bees had significantly reduced continuous flight times and prolonged resting times, other flight characteristics and navigational abilities showed no significant difference between infected and non-infected bees. Our results suggest that infected bees express normal flight characteristics but are constrained in their homing ability, potentially compromising the colony by reducing its resource inputs, but also counteracting the intra-colony spread of infection. We provide the first high-resolution analysis of sub-lethal effects of an emerging disease on insect flight behaviour. The potential causes and the implications for both host and parasite are discussed. PY - 2014 UR - https://nbn-resolving.org/urn:nbn:de:kobv:b43-328827 DO - https://doi.org/10.1371/journal.pone.0103989 SN - 1932-6203 VL - 9 IS - 8 SP - e103989, 1 EP - 15 PB - PubMed Central AN - OPUS4-32882 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - Natsopoulou, M.E. A1 - McMahon, Dino Peter A1 - Doublet, V. A1 - Bryden, J. A1 - Paxton, R.J. T1 - Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease N2 - There is increasing appreciation that hosts in natural populations are subject to infection by multiple parasite species. Yet the epidemiological and ecological processes determining the outcome of mixed infections are poorly understood. Here, we use two intracellular gut parasites (Microsporidia), one exotic and one co-evolved in the western honeybee (Apis mellifera), in an experiment in which either one or both parasites were administered either simultaneously or sequentially. We provide clear evidence of within-host competition; order of infection was an important determinant of the competitive outcome between parasites, with the first parasite significantly inhibiting the growth of the second, regardless of species. However, the strength of this 'priority effect' was highly asymmetric, with the exotic Nosema ceranae exhibiting stronger inhibition of Nosema apis than vice versa. Our results reveal an unusual asymmetry in parasite competition that is dependent on order of infection. When incorporated into a mathematical model of disease prevalence, we find asymmetric competition to be an important predictor of the patterns of parasite prevalence found in nature. Our findings demonstrate the wider significance of complex multi-host–multi-parasite interactions as drivers of host–pathogen community structure. KW - Apis mellifera KW - Microsporidia KW - Host KW - Parasite KW - Co-infection KW - Priority effect PY - 2014 DO - https://doi.org/10.1098/rspb.2014.1896 SN - 1471-2954 SN - 0950-1193 SN - 0080-4649 SN - 0962-8452 VL - 282 SP - 20141896, 1 EP - 8 PB - Royal Soc. of London CY - London AN - OPUS4-32883 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - Fürst, M.A. A1 - McMahon, Dino Peter A1 - Osborne, J.L. A1 - Paxton, R.J. A1 - Brown, M.J.F. T1 - Disease associations between honeybees and bumblebees as a threat to wild pollinators N2 - Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops2. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens3,4, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline5,6, one cause of which may be pathogen spillover from managed pollinators like honeybees7,8 or commercial colonies of bumblebees9. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates10,11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators. PY - 2014 DO - https://doi.org/10.1038/nature12977 SN - 0028-0836 SN - 1476-4687 VL - 506 SP - 364 EP - 366 PB - Nature Publishing Group CY - London AN - OPUS4-32884 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - McMahon, Dino Peter A1 - Fürst, M.A. A1 - Caspar, J. A1 - Theodorou, P. A1 - Brown, M.J.F. A1 - Paxton, R.J. T1 - A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees N2 - 1.Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. 2.This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses. 3.Within a structured large-scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co-occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. 4.Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species-specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations. 5.Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline. KW - Apis KW - Bombus KW - Decline KW - Pathogen KW - Spillover PY - 2015 DO - https://doi.org/10.1111/1365-2656.12345 SN - 1365-2656 SN - 0021-8790 VL - 84 SP - 615 EP - 624 PB - Wiley-Blackwell CY - Oxford [u.a.] AN - OPUS4-32885 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - CHAP A1 - McMahon, Dino Peter A1 - Wilfert, L. A1 - Paxton, R.J. A1 - Brown, M.J.F. T1 - Emerging viruses in bees: From molecules to ecology N2 - Emerging infectious diseases arise as a result of novel interactions between populations of hosts and pathogens, and can threaten the health and wellbeing of the entire spectrum of biodiversity. Bees andtheir viruses area case in point. However, detailed knowledge of the ecological factors and evolutionary forces that drive disease emergence in bees and other host–pathogen communities is surprisingly lacking. In this review, we build on the fundamental insight that viruses evolve and adapt over timescales that overlap with host ecology. At the same time, we integrate the role of host community ecology, including community structure and composition, biodiversity loss, and human driven disturbance, all of which represent significant factors in bee virus ecology. Both of these evolutionary and ecological perspectives represent major advances but, in most cases, it remains unclear how evolutionary forces actually operate across different biological scales (e.g., from cell to ecosystem). We present a molecule-to-ecology framework to help address these issues, emphasizing the role of molecular mechanisms as keybottom-up drivers of change at higher ecological scales. We consider the bee–virus system to be an ideal one in which to apply this framework. Unlike many other animal models, bees constitute a well characterized and accessible multispecies assemblage, whose populations and interspecific interactions can be experimentally manipulated and monitored in high resolution across space and time to provide robust tests of prevailing theory. KW - Emerging KW - Virus KW - Pathogen KW - Bee KW - Disease PY - 2018 DO - https://doi.org/10.1016/bs.aivir.2018.02.008 SN - 0065-3527 VL - 101 SP - 251 EP - 291 AN - OPUS4-46324 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - Natsopoulou, M.E. A1 - McMahon, Dino Peter A1 - Paxton, R.J. T1 - Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee N2 - Task allocation in social insect colonies is generally organised into an age-related division of labour, termed the temporal polyethism schedule, which may in part have evolved to reduce infection of the colony's brood by pests and pathogens. The temporal polyethism schedule is sensitive to colony perturbations that may lead to adaptive changes in task allocation, maintaining colony homeostasis. Though social insects can be infected by a range of parasites, little is known of how these parasites impact within-colony behaviour and the temporal polyethism schedule. We use honey bees (Apis mellifera) experimentally infected by two of their emerging pathogens, Deformed wing virus (DWV), which is relatively understudied concerning its behavioural impact on its host, and the exotic microsporidian Nosema ceranae. We examined parasite effects on host temporal polyethism and patterns of activity within the colony. We found that pathogens accelerated the temporal polyethism schedule, but without reducing host behavioural repertoire. Infected hosts exhibited increased hyperactivity, allocating more time to self-grooming and foraging-related tasks. The strength of behavioural alterations we observed was found to be pathogen specific; behavioural modifications were more pronounced in virus-treated hosts versus N. ceranae-treated hosts, with potential benefits for the colony in terms of reducing within-colony transmission. Investigating the effects of multiple pathogens on behavioural patterns of social insects could play a crucial role in understanding pathogen spread within a colony and their effects on colony social organisation. KW - Host KW - Pathogen KW - Multiple infection KW - Apis mellifera KW - Nosema ceranae KW - Deformed wing virus PY - 2016 DO - https://doi.org/10.1007/s00265-015-2019-5 SN - 0340-5443 SN - 1432-0762 VL - 70 IS - 7 SP - 1019 EP - 1031 PB - Springer CY - Berlin ; Heidelberg [u.a.] AN - OPUS4-34738 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - Doublet, V. A1 - Poeschl, Y. A1 - Gogol-Döring, A. A1 - Alaux, C. A1 - Annoscia, D. A1 - Aurori, C. A1 - Barribeau, S. M. A1 - Bedoya-Reina, O. C. A1 - Brown, M. J. F. A1 - Bull, J. C. A1 - Flenniken, M. L. A1 - Galbraith, D. A. A1 - Genersch, E. A1 - Gisder, S. A1 - Grosse, I. A1 - Holt, H. L. A1 - Hultmark, D. A1 - Lattorff, H. M. G. A1 - Le Conte, Y. A1 - Manfredini, F. A1 - McMahon, Dino Peter A1 - Moritz, R. F. A. A1 - Nazzi, F. A1 - Niño, E. L. A1 - Nowick, K. A1 - Van Rij, R. P. A1 - Paxton, R. J. A1 - Grozinger, C. M. T1 - Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens N2 - Background: Organisms typically face infection by diverse pathogens, and hosts are thought to have developed specific responses to each type of pathogen they encounter. The advent of transcriptomics now makes it possible to test this hypothesis and compare host gene expression responses to multiple pathogens at a genome-wide scale. Here, we performed a meta-analysis of multiple published and new transcriptomes using a newly developed bioinformatics approach that filters genes based on their expression profile across datasets. Thereby, we identified common and unique molecular responses of a model host species, the honey bee (Apis mellifera), to its major pathogens and parasites: the Microsporidia Nosema apis and Nosema ceranae, RNA viruses, and the ectoparasitic mite Varroa destructor, which transmits viruses. Results: We identified a common suite of genes and conserved molecular pathways that respond to all investigated pathogens, a result that suggests a commonality in response mechanisms to diverse pathogens. We found that genes differentially expressed after infection exhibit a higher evolutionary rate than non-differentially expressed genes. Using our new bioinformatics approach, we unveiled additional pathogen-specific responses of honey bees; we found that apoptosis appeared to be an important response following microsporidian infection, while genes from the immune signalling pathways, Toll and Imd, were differentially expressed after Varroa/virus infection. Finally, we applied our bioinformatics approach and generated a gene co-expression network to identify highly connected (hub) genes that may represent important mediators and regulators of anti-pathogen responses. Conclusions: Our meta-analysis generated a comprehensive overview of the host metabolic and other biological processes that mediate interactions between insects and their pathogens. We identified key host genes and pathways that respond to phylogenetically diverse pathogens, representing an important source for future functional studies as well as offering new routes to identify or generate pathogen resilient honey bee stocks. The statistical and bioinformatics approaches that were developed for this study are broadly applicable to synthesize information across transcriptomic datasets. These approaches will likely have utility in addressing a variety of biological questions. KW - Coexpression KW - Apis mellifera KW - Nosema KW - Varroa destructor KW - DWV KW - IAPV KW - RNA virus KW - Meta-analysis KW - Transcriptomics PY - 2017 UR - https://nbn-resolving.org/urn:nbn:de:kobv:b43-410439 DO - https://doi.org/10.1186/s12864-017-3597-6 SN - 1471-2164 VL - 18 SP - 207 EP - 224 AN - OPUS4-41043 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - Natsopoulou, M. E. A1 - McMahon, Dino Peter A1 - Doublet, V. A1 - Frey, E. A1 - Rosenkranz, P. A1 - Paxton, R. J. T1 - The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss N2 - Bees are considered to be threatened globally, with severe overwinter losses of the most important commercial pollinator, the Western honeybee, a major concern in the Northern Hemisphere. Emerging infectious diseases have risen to prominence due to their temporal correlation with colony losses. Among these is Deformed wing virus (DWV), which has been frequently linked to colony mortality. We now provide evidence of a strong statistical association between overwintering colony decline in the field and the presence of DWV genotype-B (DWV-B), a genetic variant of DWV that has recently been shown to be more virulent than the original DWV genotype-A. We link the prevalence of DWV-B directly to a quantitative measure of overwinter decline (workforce mortality) of honeybee colonies in the field. We demonstrate that increased prevalence of virus infection in individual bees is associated with higher overwinter mortality. We also observed a substantial reduction of infected colonies in the spring, suggesting that virus-infected individuals had died during the winter. Our findings demonstrate that DWV-B, plus possible A/B recombinants exhibiting DWV-B at PCR primer binding sites, may be a major cause of elevated overwinter honeybee loss. Its potential emergence in naïve populations of bees may have far-reaching ecological and economic impacts. KW - Honeybee KW - Loss KW - Virulence KW - Virus PY - 2017 UR - https://nbn-resolving.org/urn:nbn:de:kobv:b43-410446 DO - https://doi.org/10.1038/s41598-017-05596-3 SN - 2045-2322 IS - 7 SP - 5242, 1 EP - 5242, 9 AN - OPUS4-41044 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER - TY - JOUR A1 - McMahon, Dino Peter A1 - Natsopoulou, M. E. A1 - Doublet, V. A1 - Fürst, M. A1 - Weging, S. A1 - Brown, M. J. F. A1 - Gogol-Döring, A. A1 - Paxton, R. J. T1 - Elevated virulence of an emerging viral genotype as a driver of honeybee loss N2 - Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline. KW - Virulence KW - Emerging infectious disease KW - Pollinator KW - Decline PY - 2016 UR - https://nbn-resolving.org/urn:nbn:de:kobv:b43-368030 DO - https://doi.org/10.1098/rspb.2016.0811 SN - 0962-8452 VL - 283 IS - 1833 SP - Article 0811, 1 EP - 8 AN - OPUS4-36803 LA - eng AD - Bundesanstalt fuer Materialforschung und -pruefung (BAM), Berlin, Germany ER -