The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge

Laughton, Alice M.; Boots, Michael; Siva‐Jothy, Michael T.

doi:10.1016/j.jinsphys.2011.04.020

Cited by 94 publications

(114 citation statements)

References 67 publications

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“…The highest levels of PO activity were noted in newly emerged individuals. In our study, the results noted in healthy individuals differed significantly from those reported by Laughton et al (2011). The noted difference could result from the fact that PO activity was measured in whole bee-body extracts in different developmental stages and not in the hemolymph, as in earlier studies.…”

Section: Discussioncontrasting

confidence: 92%

“…Laughton et al (2011) observed an increase in PO activity in successive development stages of A. mellifera workers and drones. The highest levels of PO activity were noted in newly emerged individuals.…”

Section: Discussionmentioning

confidence: 84%

“…The noted difference could result from the fact that PO activity was measured in whole bee-body extracts in different developmental stages and not in the hemolymph, as in earlier studies. Laughton et al (2011) reported a significant decrease in enzyme activity in all age groups, excluding L5 workers, after bacterial lipopolysaccharide had been administered to stimulate the immune system of the studied brood. In our study, enzyme activity was also generally lower in infected brood of both sexes than in healthy individuals.…”

Section: Discussionmentioning

confidence: 86%

“…There are several causes for the decline of the bee populations, including exposure to agricultural chemicals such as pesticides (Krupke et al, 2012). Bee breeding in large apiaries of thousands of colonies can contribute to the spread of viral, bacterial, fungal, and parasitic diseases (Wilson-Rich et al, 2008;Laughton et al, 2011). The most widespread parasitic disease in bee colonies is caused by the ectoparasite Varroa destructor, a vector of dangerous pathogens for bees (vanEngelsdorp et al, 2009;Rosenkranz et al, 2010).…”

mentioning

confidence: 99%

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Expression of the Prophenoloxidase Gene and Phenoloxidase Activity, During the Development of Apis Mellifera Brood Infected with Varroa Destructor

Zaobidna

Zoltowska

Łopieńska–Biernat

2015

Journal of Apicultural Science

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A b s t r a c t The pathogenesis of varroasis has not been fully explained despite intensive research. Earlier studies suggested that parasitic infections caused by Varroa destructor mites were accompanied by immunosuppression in the host organism. The objective of this study was to analyse the influence of varroasis on one of the immune pathway in Apis mellifera measured by the expression of the prophenoloxidase (proPO) gene and the enzymatic activity of this gene's product, phenoloxidase (EC 1.14.18.1). An evaluation was done of five developmental stages of honey bee workers and drones. The relative expression of proPO decreased in infected individuals. The only exceptions were worker prepupae (PP) and drone pupae with brown eyes and dark brown thorax (P5) where propo gene expression was 1.8-fold and 1.5-fold higher, respectively, than in the control. Phenoloxidase (PO) activity was 2.8-fold higher in infected pp workers and 2-fold higher in p5 drones in comparison with uninfected bees. Phenoloxidase activity was reduced in the remaining developmental stages of infected workers and drones. The relative expression of proPO was positively correlated with the relative PO activity in both workers (r = 0.988) and drones (r = 0.996). The results of the study indicate that V. destructor significantly influences the phenoloxidase-dependent immune pathway in honey bees.Keywords: Apis mellifera, phenoloxidase activity, prophenoloxidase gen expression, Varroa destructor.University of Warmia and Mazury, Faculty of Biology and Biotechnology, Department of Biochemistry, Oczapowski 1A, 10-957 Olsztyn, Poland INTRODUCTIONThe honey bee (Apis mellifera) is an economically important pollinator whose population has been dramatically reduced in the past decades (Genersch, 2010). There are several causes for the decline of the bee populations, including exposure to agricultural chemicals such as pesticides (Krupke et al., 2012). Bee breeding in large apiaries of thousands of colonies can contribute to the spread of viral, bacterial, fungal, and parasitic diseases (Wilson-Rich et al., 2008;Laughton et al., 2011). The most widespread parasitic disease in bee colonies is caused by the ectoparasite Varroa destructor, a vector of dangerous pathogens for bees (vanEngelsdorp et al., 2009;Rosenkranz et al., 2010). By feeding on the hemolymph, V. destructor weakens the bees and depletes their food reserves, which has particularly serious consequences for wintering insects. The parasite also induces immunosuppression in the host organism. Some studies have demonstrated that immunosuppression is closely linked with varroasis (Gregory et al., 2005;Yang and Cox-Foster, 2005;Aronstein et al., 2012 Expression of proPO in A. mellifera waxes, and proteolytic enzymes which provide bees with antimicrobial protection (Strachecka et al., 2010;. Phenoloxidase mediates the nodulation or encapsulation of foreign organisms. This action prevents the development and spread of pathogens in the host's body. The enzyme also participates in wound healing, which...

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Section: Discussioncontrasting

confidence: 92%

Section: Discussionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 86%

mentioning

confidence: 99%

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Expression of the Prophenoloxidase Gene and Phenoloxidase Activity, During the Development of Apis Mellifera Brood Infected with Varroa Destructor

Zaobidna

Zoltowska

Łopieńska–Biernat

2015

Journal of Apicultural Science

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“…Difficulties in predicting outcomes lie not only in the need to understand the direct impact of temperature on individual components, but to also review the system as a whole, taking into account the dynamic nature of the selective pressures acting on life‐history trade‐offs across time (Alto & Bettinardi, 2013; Blanford, Thomas, Pugh, & Pell, 2003; Holland & Bourke, 2015; Laughton, Boots, & Siva‐Jothy, 2011). For example, higher temperatures may increase voltinism, potentially enabling host populations to rapidly adapt to thermal changes and infecting pathogens (Overgaard & Sørensen, 2008), but this may be tempered by reduced survival under temperature stress.…”

Section: Discussionmentioning

confidence: 99%

Responses to a warming world: Integrating life history, immune investment, and pathogen resistance in a model insect species

Laughton

O'Connor

Knell

2017

Ecology and Evolution

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Environmental temperature has important effects on the physiology and life history of ectothermic animals, including investment in the immune system and the infectious capacity of pathogens. Numerous studies have examined individual components of these complex systems, but little is known about how they integrate when animals are exposed to different temperatures. Here, we use the Indian meal moth (Plodia interpunctella) to understand how immune investment and disease resistance react and potentially trade‐off with other life‐history traits. We recorded life‐history (development time, survival, fecundity, and body size) and immunity (hemocyte counts, phenoloxidase activity) measures and tested resistance to bacterial (E. coli) and viral (Plodia interpunctella granulosis virus) infection at five temperatures (20–30°C). While development time, lifespan, and size decreased with temperature as expected, moths exhibited different reproductive strategies in response to small changes in temperature. At cooler temperatures, oviposition rates were low but tended to increase toward the end of life, whereas warmer temperatures promoted initially high oviposition rates that rapidly declined after the first few days of adult life. Although warmer temperatures were associated with strong investment in early reproduction, there was no evidence of an associated trade‐off with immune investment. Phenoloxidase activity increased most at cooler temperatures before plateauing, while hemocyte counts increased linearly with temperature. Resistance to bacterial challenge displayed a complex pattern, whereas survival after a viral challenge increased with rearing temperature. These results demonstrate that different immune system components and different pathogens can respond in distinct ways to changes in temperature. Overall, these data highlight the scope for significant changes in immunity, disease resistance, and host–parasite population dynamics to arise from small, biologically relevant changes to environmental temperature. In light of global warming, understanding these complex interactions is vital for predicting the potential impact of insect disease vectors and crop pests on public health and food security.

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Alate susceptibility in ants

Frederickson

2014

Ecology and Evolution

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Pathogens are predicted to pose a particular threat to eusocial insects because infections can spread rapidly in colonies with high densities of closely related individuals. In ants, there are two major castes: workers and reproductives. Sterile workers receive no direct benefit from investing in immunity, but can gain indirect fitness benefits if their immunity aids the survival of their fertile siblings. Virgin reproductives (alates), on the other hand, may be able to increase their investment in reproduction, rather than in immunity, because of the protection they receive from workers. Thus, we expect colonies to have highly immune workers, but relatively more susceptible alates. We examined the survival of workers, gynes, and males of nine ant species collected in Peru and Canada when exposed to the entomopathogenic fungus Beauveria bassiana. For the seven species in which treatment with B. bassiana increased ant mortality relative to controls, we found workers were significantly less susceptible compared with both alate sexes. Female and male alates did not differ significantly in their immunocompetence. Our results suggest that, as with other nonreproductive tasks in ant colonies like foraging and nest maintenance, workers have primary responsibility for colony immunity, allowing alates to specialize on reproduction. We highlight the importance of colony-level selection on individual immunity in ants and other eusocial organisms.

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The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge

Cited by 94 publications

References 67 publications

Expression of the Prophenoloxidase Gene and Phenoloxidase Activity, During the Development of Apis Mellifera Brood Infected with Varroa Destructor

Expression of the Prophenoloxidase Gene and Phenoloxidase Activity, During the Development of Apis Mellifera Brood Infected with Varroa Destructor

Responses to a warming world: Integrating life history, immune investment, and pathogen resistance in a model insect species

Alate susceptibility in ants

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