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 - Mayack, C. A1 - Natsopoulou, M.E. A1 - McMahon, Dino Peter T1 - Nosema ceranae alters a highly conserved hormonal stress pathway in honeybees N2 - Nosema ceranae, an emerging pathogen of the western honeybee (Apis mellifera), is implicated in recent pollinator losses and causes severe energetic stress. However, whether precocious foraging and accelerated behavioural maturation in infected bees are caused by the infection itself or via indirect energetic stress remains unknown. Using a combination of nutritional and infection treatments, we investigated how starvation and infection alters the regulation of adipokinetic hormone (AKH) and octopamine, two highly conserved physiological pathways that respond to energetic stress by mobilizing fat stores and increasing search activity for food. Although there was no response from AKH when bees were experimentally infected with N. ceranae or starved, supporting the notion that honeybees have lost this pathway, there were significant regulatory changes in the octopamine pathway. Significantly, we found no evidence of acute energetic stress being the only cause of symptoms associated with N. ceranae infection. Therefore, the parasite itself appears to alter regulatory components along a highly conserved physiological pathway in an infection-specific manner. This indicates that pathogen-induced behavioural alteration of chronically infected bees should not just be viewed as a coincidental short-term by-product of pathogenesis (acute energetic stress) and may be a result of a generalist manipulation strategy to obtain energy for reproduction. KW - Octopamine KW - Adipokinetic hormone (AKH) KW - Apis mellifera KW - Energetic stress KW - Starvation KW - Hunger PY - 2015 DO - https://doi.org/10.1111/imb.12190 SN - 0962-1075 SN - 1365-2583 SP - 1 EP - 9 PB - Blackwell CY - Oxford AN - OPUS4-34168 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 -