Biology of Social Insect Diseases

A topical collection in Insects (ISSN 2075-4450). This collection belongs to the section "Insect Behavior and Pathology".

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Editor


E-Mail Website
Collection Editor
Institute for Bee Protection, Julius Kühn-Institut, Messeweg 11/12, 38104 Braunschweig, Germany
Interests: host-parasite interaction; social insects; honey bees; bumble bees; innate immunity; social immunity; self-medication; ecology; physiology; nutritional immunology; pathogens; microbiome; plant protection products; ecotoxicology

Topical Collection Information

Dear Colleagues,

Social insects are a highly diverse group of animals exhibiting different lifestyles and kinds of social organization. Their ecological success, however, means that they are also a highly attractive target for an equally diverse set of parasites and pathogens. In this Topical Collection (former Special Issue), we will focus on the prevention, infection, transmission, and dynamics of social insect diseases caused by microorganisms. We welcome recent discoveries and reviews that aim at understanding potential mechanisms driving the spread or course of disease and preventing or suppressing disease outbreaks in social insect hosts at the individual, group, or colony level. Molecular, chemical, physiological, and ecological mechanisms explaining mechanisms of social insect disease biology are clearly within the focus of this thematic issue. Please contact me (Silvio Erler), prior to submission, if you are unsure whether your manuscript falls within the aims and scope of this Topical Collection.

Dr. Silvio Erler
Collection Editor

Manuscript Submission Information

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Keywords

  • social insects
  • host-parasite interactions
  • ecology
  • evolution
  • physiology
  • innate immunity
  • nutritional immunology
  • behavioral defence
  • pathogens
  • microorganisms

Published Papers (21 papers)

2023

Jump to: 2022, 2020, 2019

15 pages, 4792 KiB  
Article
Biotechnical Control of Varroa in Honey Bee Colonies: A Trade-Off between Sustainable Beekeeping and Profitability?
by Monica Vercelli, Luca Croce and Teresina Mancuso
Insects 2023, 14(10), 830; https://doi.org/10.3390/insects14100830 - 23 Oct 2023
Cited by 2 | Viewed by 2963
Abstract
Beekeeping faces several challenges, such as the Varroa mite. Few studies have measured the economic performance of farms in relation to the practices used for Varroa control. Our study analyzed various biotechniques (total brood removal, TBR; queen caging, QC; royal cell insertion, CI) [...] Read more.
Beekeeping faces several challenges, such as the Varroa mite. Few studies have measured the economic performance of farms in relation to the practices used for Varroa control. Our study analyzed various biotechniques (total brood removal, TBR; queen caging, QC; royal cell insertion, CI) and other methods (chemical treatments, CT; thymol use, THY) adopted by Italian beekeepers to show whether the adoption of biotechniques leads to farm profitability or a necessary trade-off between sustainability and profitability. Beekeepers were interviewed about the methods and operations conducted on their farms. The net incomes (NIs) of the farms were calculated and inter- and intrafarm comparisons were performed. A detailed schema of each practice was designed. The net income derived from TBR was the highest in eight out of the nine case studies, followed by CI and then QC. The NI calculated for farms using CT was lower than that for farms using other methods in two of the case studies. We also analyzed different biotechniques applied by the same farm and found that the NI resulting from TBR was higher than that achieved from the use of QC and CI. Our study suggests that use of biotechniques represents a long-term sustainable solution for reducing the level of Varroa infestation, which affects farm net income. Full article
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12 pages, 2058 KiB  
Article
Co-Occurrence of Wing Deformity and Impaired Mobility of Alates with Deformed Wing Virus in Solenopsis invicta Buren (Hymenoptera: Formicidae)
by Godfrey P. Miles, Xiaofen F. Liu, Esmaeil Amiri, Michael J. Grodowitz, Margaret L. Allen and Jian Chen
Insects 2023, 14(10), 788; https://doi.org/10.3390/insects14100788 - 27 Sep 2023
Cited by 3 | Viewed by 3085
Abstract
Deformed wing virus (DWV), a major honey bee pathogen, is a generalist insect virus detected in diverse insect phyla, including numerous ant genera. Its clinical symptoms have only been reported in honey bees, bumble bees, and wasps. DWV is a quasispecies virus with [...] Read more.
Deformed wing virus (DWV), a major honey bee pathogen, is a generalist insect virus detected in diverse insect phyla, including numerous ant genera. Its clinical symptoms have only been reported in honey bees, bumble bees, and wasps. DWV is a quasispecies virus with three main variants, which, in association with the ectoparasitic mite, Varroa destructor, causes wing deformity, shortened abdomens, neurological impairments, and colony mortality in honey bees. The red imported fire ant, Solenopsis invicta Buren, is one of the most-invasive and detrimental pests in the world. In this study, we report the co-occurrence of DWV-like symptoms in S. invicta and DWV for the first time and provide molecular evidence of viral replication in S. invicta. Some alates in 17 of 23 (74%) lab colonies and 9 of 14 (64%) field colonies displayed deformed wings (DWs), ranging from a single crumpled wing tip to twisted, shriveled wings. Numerous symptomatic alates also exhibited altered locomotion ranging from an altered gait to the inability to walk. Deformed wings may prevent S. invicta alates from reproducing since mating only occurs during a nuptial flight. The results from conventional RT-PCR and Sanger sequencing confirmed the presence of DWV-A, and viral replication of DWV was confirmed using a modified strand-specific RT-PCR. Our results suggest that S. invicta can potentially be an alternative and reservoir host for DWV. However, further research is needed to determine whether DWV is the infectious agent that causes the DW syndrome in S. invicta. Full article
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2022

Jump to: 2023, 2020, 2019

13 pages, 2510 KiB  
Article
The Role of Honey Bee Derived Aliphatic Esters in the Host-Finding Behavior of Varroa destructor
by Jiamei Liu, Ruonan Zhang, Rui Tang, Yi Zhang, Rui Guo, Guojun Xu, Dafu Chen, Zachary Y. Huang, Yanping Chen, Richou Han and Wenfeng Li
Insects 2023, 14(1), 24; https://doi.org/10.3390/insects14010024 - 25 Dec 2022
Cited by 8 | Viewed by 3031
Abstract
Varroa destructor is an obligate ectoparasite of honey bees and shifted from its original host Apis cerana to the new host Apis mellifera in the first half of the twentieth century. The host shift has resulted in a great threat to the health [...] Read more.
Varroa destructor is an obligate ectoparasite of honey bees and shifted from its original host Apis cerana to the new host Apis mellifera in the first half of the twentieth century. The host shift has resulted in a great threat to the health and survival of A. mellifera colonies worldwide. Chemical signals play a crucial role in all aspects of the Varroa life cycle, including host finding. However, the chemical cues that affect the host finding behavior of Varroa mites are still not fully understood. In this study, we systematically profiled the headspace volatiles of both worker and drone larvae of the two honey bee species by using solid phase micro-extraction coupled to gas chromatography-mass spectrometry (SPME-GC-MS), and then used electrophysiological recording and Y-tube olfactometer bioassay to study the potential roles of the selected compounds. The chemical profiling showed that there were four aliphatic esters, ethyl myristate (EM), methyl palmitate (MP), ethyl palmitate (EP), and ethyl oleate (EO) commonly detected from all four types of larval hosts. Among them, EM was a new substance identified from honey bee headspace volatiles. Results from electrophysiological recordings indicated that all the aliphatic esters could elicit significant responses of Varroa pit organs on its forelegs. Moreover, behavioral analyses revealed that EM could significantly attract V. destructor at a medium dosage (10 µg), while MP had no observable effect on the mites and both EP and EO were able to repel the parasites. Our findings suggest an important role of host-derived aliphatic esters in Varroa host finding, and provide new chemicals for Varroa monitoring and control. Full article
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18 pages, 2962 KiB  
Article
Identity, Prevalence, and Pathogenicity of Entomopathogenic Fungi Infecting Invasive Polistes (Vespidae: Polistinae) Paper Wasps in New Zealand
by Aiden Reason, Mariana Bulgarella and Philip J. Lester
Insects 2022, 13(10), 922; https://doi.org/10.3390/insects13100922 - 12 Oct 2022
Cited by 2 | Viewed by 3430
Abstract
Two species of entomogenous fungi were discovered infecting the invasive paper wasp Polistes chinensis during an ecological study on Farewell Spit, New Zealand. We sequenced two nuclear ribosomal RDNA genes, the internal transcribed spacer (ITS) and the small ribosomal subunit 18S, and one [...] Read more.
Two species of entomogenous fungi were discovered infecting the invasive paper wasp Polistes chinensis during an ecological study on Farewell Spit, New Zealand. We sequenced two nuclear ribosomal RDNA genes, the internal transcribed spacer (ITS) and the small ribosomal subunit 18S, and one protein-coding gene, the translation elongation factor 1-alpha (ef1 α). Combining sequence information with morphological examination, we identified these species as Beauveria malawiensis and Ophiocordyceps humbertii. We estimated that these fungi produce infection in approximately 3.3% of colonies in our study population. In bioassays, we successfully infected P. chinensis individuals from healthy colonies with B. malawiensis, with significant effects on adult mortality. This is the first record of both B. malawiensis and O. humbertii from Polistine hosts in New Zealand, and the first investigation into disease causality by these pathogens in P. chinensis. Our findings may contribute to the future development of biological control agents for paper wasps in New Zealand and elsewhere around the world. Full article
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2020

Jump to: 2023, 2022, 2019

20 pages, 1133 KiB  
Review
Pollutants and Their Interaction with Diseases of Social Hymenoptera
by Heike Feldhaar and Oliver Otti
Insects 2020, 11(3), 153; https://doi.org/10.3390/insects11030153 - 1 Mar 2020
Cited by 58 | Viewed by 14411
Abstract
Many insect species, including social insects, are currently declining in abundance and diversity. Pollutants such as pesticides, heavy metals, or airborne fine particulate matter from agricultural and industrial sources are among the factors driving this decline. While these pollutants can have direct detrimental [...] Read more.
Many insect species, including social insects, are currently declining in abundance and diversity. Pollutants such as pesticides, heavy metals, or airborne fine particulate matter from agricultural and industrial sources are among the factors driving this decline. While these pollutants can have direct detrimental effects, they can also result in negative interactive effects when social insects are simultaneously exposed to multiple stressors. For example, sublethal effects of pollutants can increase the disease susceptibility of social insects, and thereby jeopardize their survival. Here we review how pesticides, heavy metals, or airborne fine particulate matter interact with social insect physiology and especially the insects’ immune system. We then give an overview of the current knowledge of the interactive effects of these pollutants with pathogens or parasites. While the effects of pesticide exposure on social insects and their interactions with pathogens have been relatively well studied, the effects of other pollutants, such as heavy metals in soil or fine particulate matter from combustion, vehicular transport, agriculture, and coal mining are still largely unknown. We therefore provide an overview of urgently needed knowledge in order to mitigate the decline of social insects. Full article
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16 pages, 1415 KiB  
Article
Relish as a Candidate Marker for Transgenerational Immune Priming in a Dampwood Termite (Blattodae: Archeotermopsidae)
by Erin L. Cole, Jessica S. Empringham, Colette Biro, Graham J. Thompson and Rebeca B. Rosengaus
Insects 2020, 11(3), 149; https://doi.org/10.3390/insects11030149 - 27 Feb 2020
Cited by 8 | Viewed by 3618
Abstract
Natural selection should favor the transfer of immune competence from one generation to the next in a context-dependent manner. Transgenerational immune priming (TGIP) is expected to evolve when species exploit pathogen-rich environments and exhibit extended overlap of parent–offspring generations. Dampwood termites are hemimetabolous, [...] Read more.
Natural selection should favor the transfer of immune competence from one generation to the next in a context-dependent manner. Transgenerational immune priming (TGIP) is expected to evolve when species exploit pathogen-rich environments and exhibit extended overlap of parent–offspring generations. Dampwood termites are hemimetabolous, eusocial insects (Blattodea: Archeotermopsidae) that possess both of these traits. We predict that offspring of pathogen-exposed queens of Zootermopsis angusticollis will show evidence of a primed immune system relative to the offspring of unexposed controls. We found that Relish transcripts, one of two immune marker loci tested, were enhanced in two-day-old embryos when laid by Serratia-injected queens. These data implicate the immune deficiency (IMD) signaling pathway in TGIP. Although an independent antibacterial assay revealed that embryos do express antibacterial properties, these do not vary as a function of parental treatment. Taken together, Z. angusticollis shows transcriptional but not translational evidence for TGIP. This apparent incongruence between the transcriptional and antimicrobial response from termites suggests that effectors are either absent in two-day-old embryos or their activity is too subtle to detect with our antibacterial assay. In total, we provide the first suggestive evidence of transgenerational immune priming in a termite. Full article
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2019

Jump to: 2023, 2022, 2020

10 pages, 3578 KiB  
Article
The Association between Virus Prevalence and Intercolonial Aggression Levels in the Yellow Crazy Ant, Anoplolepis Gracilipes (Jerdon)
by Hung-Wei Hsu, Ming-Chung Chiu, Ching-Chen Lee, Chow-Yang Lee and Chin-Cheng Scotty Yang
Insects 2019, 10(12), 436; https://doi.org/10.3390/insects10120436 - 4 Dec 2019
Cited by 8 | Viewed by 3558
Abstract
The recent discovery of multiple viruses in ants, along with the widespread infection of their hosts across geographic ranges, provides an excellent opportunity to test whether viral prevalence in the field is associated with the complexity of social interactions in the ant population. [...] Read more.
The recent discovery of multiple viruses in ants, along with the widespread infection of their hosts across geographic ranges, provides an excellent opportunity to test whether viral prevalence in the field is associated with the complexity of social interactions in the ant population. In this study, we examined whether the association exists between the field prevalence of a virus and the intercolonial aggression of its ant host, using the yellow crazy ant (Anoplolepis gracilipes) and its natural viral pathogen (TR44839 virus) as a model system. We delimitated the colony boundary and composition of A. gracilipes in a total of 12 study sites in Japan (Okinawa), Taiwan, and Malaysia (Penang), through intercolonial aggression assay. The spatial distribution and prevalence level of the virus was then mapped for each site. The virus occurred at a high prevalence in the surveyed colonies of Okinawa and Taiwan (100% infection rate across all sites), whereas virus prevalence was variable (30%–100%) or none (0%) at the sites in Penang. Coincidentally, colonies in Okinawa and Taiwan displayed a weak intercolonial boundary, as aggression between colonies is generally low or moderate. Contrastingly, sites in Penang were found to harbor a high proportion of mutually aggressive colonies, a pattern potentially indicative of complex colony composition. Our statistical analyses further confirmed the observed correlation, implying that intercolonial interactions likely contribute as one of the effective facilitators of/barriers to virus prevalence in the field population of this ant species. Full article
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17 pages, 976 KiB  
Article
Age and Method of Inoculation Influence the Infection of Worker Honey Bees (Apis mellifera) by Nosema ceranae
by Almudena Urbieta-Magro, Mariano Higes, Aránzazu Meana, Laura Barrios and Raquel Martín-Hernández
Insects 2019, 10(12), 417; https://doi.org/10.3390/insects10120417 - 22 Nov 2019
Cited by 15 | Viewed by 3622
Abstract
The microsporidian parasite Nosema ceranae is a highly prevalent, global honey bee pathogen. Apis mellifera is considered to be a relatively recent host for this microsporidia, which raises questions as to how it affects its host’s physiology, behavior and longevity, both at the [...] Read more.
The microsporidian parasite Nosema ceranae is a highly prevalent, global honey bee pathogen. Apis mellifera is considered to be a relatively recent host for this microsporidia, which raises questions as to how it affects its host’s physiology, behavior and longevity, both at the individual and colony level. As such, honey bees were inoculated with fresh purified spores of this pathogen, both individually (Group A) or collectively (Group B) and they were studied from 0 to 15 days post-emergence (p.e.) to evaluate the effect of bee age and the method of inoculation at 7 days post-infection. The level of infection was analyzed individually by qPCR by measuring the relative amount of the N. ceranae polar tubule protein 3 (PTP3) gene. The results show that the bee’s age and the method of infection directly influence parasite load, and thus, early disease development. Significant differences were found regarding bee age at the time of infection, whereby the youngest bees (new-born and 1 day p.e.) developed the highest parasite load, with this load decreasing dramatically in bees infected at 2 days p.e. before increasing again in bees infected at 3–4 days p.e. The parasite load in bees infected when older than 4 days p.e. diminished as they aged. When the age cohort data was pooled and grouped according to the method of infection, a significantly higher mean concentration and lower variation in N. ceranae infection was evident in Group A, indicating greater variation in experimental infection when spores were administered collectively to bees through their food. In summary, these data indicate that both biological and experimental factors should be taken into consideration when comparing data published in the literature. Full article
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29 pages, 768 KiB  
Review
Towards Precision Nutrition: A Novel Concept Linking Phytochemicals, Immune Response and Honey Bee Health
by Pedro Negri, Ethel Villalobos, Nicolás Szawarski, Natalia Damiani, Liesel Gende, Melisa Garrido, Matías Maggi, Silvina Quintana, Lorenzo Lamattina and Martin Eguaras
Insects 2019, 10(11), 401; https://doi.org/10.3390/insects10110401 - 12 Nov 2019
Cited by 32 | Viewed by 5777
Abstract
The high annual losses of managed honey bees (Apis mellifera) has attracted intensive attention, and scientists have dedicated much effort trying to identify the stresses affecting bees. There are, however, no simple answers; rather, research suggests multifactorial effects. Several works have [...] Read more.
The high annual losses of managed honey bees (Apis mellifera) has attracted intensive attention, and scientists have dedicated much effort trying to identify the stresses affecting bees. There are, however, no simple answers; rather, research suggests multifactorial effects. Several works have been reported highlighting the relationship between bees’ immunosuppression and the effects of malnutrition, parasites, pathogens, agrochemical and beekeeping pesticides exposure, forage dearth and cold stress. Here we analyze a possible connection between immunity-related signaling pathways that could be involved in the response to the stress resulted from Varroa-virus association and cold stress during winter. The analysis was made understanding the honey bee as a superorganism, where individuals are integrated and interacting within the colony, going from social to individual immune responses. We propose the term “Precision Nutrition” as a way to think and study bees’ nutrition in the search for key molecules which would be able to strengthen colonies’ responses to any or all of those stresses combined. Full article
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13 pages, 1166 KiB  
Article
Reproduction of Distinct Varroa destructor Genotypes on Honey Bee Worker Brood
by Wenfeng Li, Cheng Wang, Zachary Y. Huang, Yanping Chen and Richou Han
Insects 2019, 10(11), 372; https://doi.org/10.3390/insects10110372 - 25 Oct 2019
Cited by 10 | Viewed by 3461
Abstract
Honey bees play important roles in pollination for many crops and wild plants, but have been facing great threats posed by various pathogens and parasites. Among them, Varroa destructor, an obligate ectoparasite of honey bees, is considered the most damaging. Within the [...] Read more.
Honey bees play important roles in pollination for many crops and wild plants, but have been facing great threats posed by various pathogens and parasites. Among them, Varroa destructor, an obligate ectoparasite of honey bees, is considered the most damaging. Within the last century, V. destructor shifted from the original host, the Asian honey bee Apis cerana to the new host, the European honey bee A. mellifera. However, the reproduction of Varroa mites, especially of different haplotypes in the two hosts, is still largely unknown. In this study, we first investigated the existing Varroa haplotypes in local colonies in southern China, and then compared the reproduction of different haplotypes on the worker brood of both the original and new hosts by artificial inoculation. We confirmed that there are two haplotypes of V. destructor in southern China, one is the Korea haplotype and the other is the China haplotype, and the two types parasitized different honey bee species. Although Varroa females from A. mellifera (Korea haplotype) are able to reproduce on the worker brood of both honey bee species, they showed better reproductive performance in the new host A. mellifera with significantly higher fecundity (number of offspring per mother mite) and reproductive rate (number of adult daughters per mother mite), suggesting that this parasite gains higher fitness after host shift. The data further showed that a short stay of Varroa females inside the A. cerana worker cells decreased their fecundity and especially the reproductive rate in a time-dependent manner, suggesting that the A. cerana worker cells may inhibit Varroa reproduction. In contrast, Varroa mites derived from A. cerana colonies (China haplotype) were entirely sterile in A. mellifera worker cells during two sequential inoculations, while the control mites from A. mellifera colonies (Korea haplotype) reproduced normally. In addition, all the infertile mites were found to defecate on the abdomen of bee pupae. We have revealed that two haplotypes of V. destructor exhibit differential reproduction on the worker brood of the original and new host honey bees, providing novel insights into the diversity and complexity of the reproduction of V. destructor. Full article
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26 pages, 743 KiB  
Review
Natural Product Medicines for Honey Bees: Perspective and Protocols
by James P. Tauber, William R. Collins, Ryan S. Schwarz, Yanping Chen, Kyle Grubbs, Qiang Huang, Dawn Lopez, Raymond Peterson and Jay D. Evans
Insects 2019, 10(10), 356; https://doi.org/10.3390/insects10100356 - 18 Oct 2019
Cited by 33 | Viewed by 7593
Abstract
The western honey bee remains the most important pollinator for agricultural crops. Disease and stressors threaten honey bee populations and productivity during winter- and summertime, creating costs for beekeepers and negative impacts on agriculture. To combat diseases and improve overall bee health, researchers [...] Read more.
The western honey bee remains the most important pollinator for agricultural crops. Disease and stressors threaten honey bee populations and productivity during winter- and summertime, creating costs for beekeepers and negative impacts on agriculture. To combat diseases and improve overall bee health, researchers are constantly developing honey bee medicines using the tools of microbiology, molecular biology and chemistry. Below, we present a manifesto alongside standardized protocols that outline the development and a systematic approach to test natural products as ‘bee medicines’. These will be accomplished in both artificial rearing conditions and in colonies situated in the field. Output will be scored by gene expression data of host immunity, bee survivorship, reduction in pathogen titers, and more subjective merits of the compound in question. Natural products, some of which are already encountered by bees in the form of plant resins and nectar compounds, provide promising low-cost candidates for safe prophylaxis or treatment of bee diseases. Full article
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14 pages, 1429 KiB  
Article
Effect of Abscisic Acid (ABA) Combined with Two Different Beekeeping Nutritional Strategies to Confront Overwintering: Studies on Honey Bees’ Population Dynamics and Nosemosis
by Nicolás Szawarski, Agustín Saez, Enzo Domínguez, Rachel Dickson, Ángela De Matteis, Carlos Eciolaza, Marcelino Justel, Alfredo Aliano, Pedro Solar, Ignacio Bergara, Claudia Pons, Aldo Bolognesi, Gabriel Carna, Walter Garcia, Omar Garcia, Martin Eguaras, Lorenzo Lamattina, Matías Maggi and Pedro Negri
Insects 2019, 10(10), 329; https://doi.org/10.3390/insects10100329 - 1 Oct 2019
Cited by 14 | Viewed by 3793
Abstract
In temperate climates, beekeeping operations suffer colony losses and colony depopulation of Apis mellifera during overwintering, which are associated with biotic and abiotic stressors that impact bees’ health. In this work, we evaluate the impacts of abscisic acid (ABA) dietary supplementation on honey [...] Read more.
In temperate climates, beekeeping operations suffer colony losses and colony depopulation of Apis mellifera during overwintering, which are associated with biotic and abiotic stressors that impact bees’ health. In this work, we evaluate the impacts of abscisic acid (ABA) dietary supplementation on honey bee colonies kept in Langstroth hives. The effects of ABA were evaluated in combination with two different beekeeping nutritional strategies to confront overwintering: “honey management” and “syrup management”. Specifically, we evaluated strength parameters of honey bee colonies (adult bee and brood population) and the population dynamics of Nosema (prevalence and intensity) associated with both nutritional systems and ABA supplementation during the whole study (late autumn-winter-early spring). The entire experiment was designed and performed with a local group of beekeepers, “Azahares del sudeste”, who showed interest in answering problems associated with the management of honey bee colonies during the winter. The results indicated that the ABA supplementation had positive effects on the population dynamics of the A. mellifera colonies during overwintering and on the nosemosis at colony level (prevalence) in both nutritional strategies evaluated. Full article
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13 pages, 910 KiB  
Article
Behavioral Genetics of the Interactions between Apis mellifera and Varroa destructor
by Alexis Beaurepaire, Christina Sann, Daniela Arredondo, Fanny Mondet and Yves Le Conte
Insects 2019, 10(9), 299; https://doi.org/10.3390/insects10090299 - 16 Sep 2019
Cited by 10 | Viewed by 3802
Abstract
The western honeybee Apis mellifera exhibits a diverse set of adaptations in response to infestations by its most virulent disease-causing agent, the ectoparasitic mite Varroa destructor. In this study, we investigated the effect of honeybee pupae genotype on the expression of four [...] Read more.
The western honeybee Apis mellifera exhibits a diverse set of adaptations in response to infestations by its most virulent disease-causing agent, the ectoparasitic mite Varroa destructor. In this study, we investigated the effect of honeybee pupae genotype on the expression of four host and parasite traits that are associated with the reproductive phase of the mite in the brood of its host. We first phenotyped cells containing bee pupae to assess their infestation status, their infestation level, the reproductive status of the mites, and the recapping of cells by adult workers. We then genotyped individual pupae with five microsatellites markers to compare these phenotypes across full sister groups. We found that the four phenotypes varied significantly in time but did not across the subfamilies within the colonies. These findings show that V. destructor mites do not differentially infest or reproduce on some particular honeybee patrilines, and that workers do not target preferentially specific pupae genotypes when performing recapping. These findings bring new insights that can help designing sustainable mite control strategies through breeding and provide new insights into the interactions between A. mellifera and V. destructor. Full article
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17 pages, 699 KiB  
Article
Effects of a Resident Yeast from the Honeybee Gut on Immunity, Microbiota, and Nosema Disease
by James P. Tauber, Vy Nguyen, Dawn Lopez and Jay D. Evans
Insects 2019, 10(9), 296; https://doi.org/10.3390/insects10090296 - 13 Sep 2019
Cited by 39 | Viewed by 5343
Abstract
The western honeybee (Apis mellifera) has a core bacterial microbiota that is well described and important for health. Honeybees also host a yeast community that is poorly understood with respect to host nutrition and immunity, and also the symbiotic bacterial microbiota. [...] Read more.
The western honeybee (Apis mellifera) has a core bacterial microbiota that is well described and important for health. Honeybees also host a yeast community that is poorly understood with respect to host nutrition and immunity, and also the symbiotic bacterial microbiota. In this work, we present two studies focusing on the consequences of dysbiosis when honeybees were control-fed a yeast that was isolated from a honeybee midgut, Wickerhamomyces anomalus. Yeast augmentation for bees with developed microbiota appeared immunomodulatory (lowered immunity and hormone-related gene expression) and affected the microbial community, while yeast augmentation for newly emerged bees without an established bacterial background did not lead to decreased immunity— and hormone—related gene expression. In newly emerged bees that had a naturally occurring baseline level of W. anomalus, we observed that the addition of N. ceranae led to a decrease in yeast levels. Overall, we show that yeasts can affect the microbiome, immunity, and physiology. Full article
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14 pages, 1559 KiB  
Article
Comparison of Twelve Ant Species and Their Susceptibility to Fungal Infection
by Nick Bos, Viljami Kankaanpää-Kukkonen, Dalial Freitak, Dimitri Stucki and Liselotte Sundström
Insects 2019, 10(9), 271; https://doi.org/10.3390/insects10090271 - 26 Aug 2019
Cited by 16 | Viewed by 4524
Abstract
Eusocial insects, such as ants, have access to complex disease defenses both at the individual, and at the colony level. However, different species may be exposed to different diseases, and/or deploy different methods of coping with disease. Here, we studied and compared survival [...] Read more.
Eusocial insects, such as ants, have access to complex disease defenses both at the individual, and at the colony level. However, different species may be exposed to different diseases, and/or deploy different methods of coping with disease. Here, we studied and compared survival after fungal exposure in 12 species of ants, all of which inhabit similar habitats. We exposed the ants to two entomopathogenic fungi (Beauveria bassiana and Metarhizium brunneum), and measured how exposure to these fungi influenced survival. We furthermore recorded hygienic behaviors, such as autogrooming, allogrooming and trophallaxis, during the days after exposure. We found strong differences in autogrooming behavior between the species, but none of the study species performed extensive allogrooming or trophallaxis under the experimental conditions. Furthermore, we discuss the possible importance of the metapleural gland, and how the secondary loss of this gland in the genus Camponotus could favor a stronger behavioral response against pathogen threats. Full article
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22 pages, 6046 KiB  
Article
Comparative Identification of MicroRNAs in Apis cerana cerana Workers’ Midguts in Response to Nosema ceranae Invasion
by Dafu Chen, Yu Du, Huazhi Chen, Yuanchan Fan, Xiaoxue Fan, Zhiwei Zhu, Jie Wang, Cuiling Xiong, Yanzhen Zheng, Chunsheng Hou, Qingyun Diao and Rui Guo
Insects 2019, 10(9), 258; https://doi.org/10.3390/insects10090258 - 21 Aug 2019
Cited by 13 | Viewed by 3714
Abstract
Here, the expression profiles and differentially expressed miRNAs (DEmiRNAs) in the midguts of Apis cerana cerana workers at 7 d and 10 d post-inoculation (dpi) with N. ceranae were investigated via small RNA sequencing and bioinformatics. Five hundred and twenty nine (529) known [...] Read more.
Here, the expression profiles and differentially expressed miRNAs (DEmiRNAs) in the midguts of Apis cerana cerana workers at 7 d and 10 d post-inoculation (dpi) with N. ceranae were investigated via small RNA sequencing and bioinformatics. Five hundred and twenty nine (529) known miRNAs and 25 novel miRNAs were identified in this study, and the expression of 16 predicted miRNAs was confirmed by Stem-loop RT-PCR. A total of 14 DEmiRNAs were detected in the midgut at 7 dpi, including eight up-regulated and six down-regulated miRNAs, while 12 DEmiRNAs were observed in the midgut at 10 dpi, including nine up-regulated and three down-regulated ones. Additionally, five DEmiRNAs were shared, while nine and seven DEmiRNAs were specifically expressed in midguts at 7 dpi and 10 dpi. Gene ontology analysis suggested some DEmiRNAs and corresponding target mRNAs were involved in various functions including immune system processes and response to stimulus. KEGG pathway analysis shed light on the potential functions of some DEmiRNAs in regulating target mRNAs engaged in material and energy metabolisms, cellular immunity and the humoral immune system. Further investigation demonstrated a complex regulation network between DEmiRNAs and their target mRNAs, with miR-598-y, miR-252-y, miR-92-x and miR-3654-y at the center. Our results can facilitate future exploration of the regulatory roles of miRNAs in host responses to N. ceranae, and provide potential candidates for further investigation of the molecular mechanisms underlying eastern honeybee-microsporidian interactions. Full article
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26 pages, 4168 KiB  
Article
Genome-Wide Identification of Long Non-Coding RNAs and Their Regulatory Networks Involved in Apis mellifera ligustica Response to Nosema ceranae Infection
by Dafu Chen, Huazhi Chen, Yu Du, Dingding Zhou, Sihai Geng, Haipeng Wang, Jieqi Wan, Cuiling Xiong, Yanzhen Zheng and Rui Guo
Insects 2019, 10(8), 245; https://doi.org/10.3390/insects10080245 - 9 Aug 2019
Cited by 39 | Viewed by 4808
Abstract
Long non-coding RNAs (lncRNAs) are a diverse class of transcripts that structurally resemble mRNAs but do not encode proteins, and lncRNAs have been proven to play pivotal roles in a wide range of biological processes in animals and plants. However, knowledge of expression [...] Read more.
Long non-coding RNAs (lncRNAs) are a diverse class of transcripts that structurally resemble mRNAs but do not encode proteins, and lncRNAs have been proven to play pivotal roles in a wide range of biological processes in animals and plants. However, knowledge of expression patterns and potential roles of honeybee lncRNA response to Nosema ceranae infection is completely unknown. Here, we performed whole transcriptome strand-specific RNA sequencing of normal midguts of Apis mellifera ligustica workers (Am7CK, Am10CK) and N. ceranae-inoculated midguts (Am7T, Am10T), followed by comprehensive analyses using bioinformatic and molecular approaches. A total of 6353 A. m. ligustica lncRNAs were identified, including 4749 conserved lncRNAs and 1604 novel lncRNAs. These lncRNAs had minimal sequence similarities with other known lncRNAs in other species; however, their structural features were similar to counterparts in mammals and plants, including shorter exon and intron length, lower exon number, and lower expression level, compared with protein-coding transcripts. Further, 111 and 146 N. ceranae-responsive lncRNAs were identified from midguts at 7-days post-inoculation (dpi) and 10 dpi compared with control midguts. Twelve differentially expressed lncRNAs (DElncRNAs) were shared by Am7CK vs. Am7T and Am10CK vs. Am10T comparison groups, while the numbers of unique DElncRNAs were 99 and 134, respectively. Functional annotation and pathway analysis showed that the DElncRNAs may regulate the expression of neighboring genes by acting in cis and trans fashion. Moreover, we discovered 27 lncRNAs harboring eight known miRNA precursors and 513 lncRNAs harboring 2257 novel miRNA precursors. Additionally, hundreds of DElncRNAs and their target miRNAs were found to form complex competitive endogenous RNA (ceRNA) networks, suggesting that these DElncRNAs may act as miRNA sponges. Furthermore, DElncRNA-miRNA-mRNA networks were constructed and investigated, the results demonstrated that a portion of the DElncRNAs were likely to participate in regulating the host material and energy metabolism as well as cellular and humoral immune host responses to N. ceranae invasion. Our findings revealed here offer not only a rich genetic resource for further investigation of the functional roles of lncRNAs involved in the A. m. ligustica response to N. ceranae infection, but also a novel insight into understanding the host-pathogen interaction during honeybee microsporidiosis. Full article
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11 pages, 1035 KiB  
Article
Subterranean Termite Social Alarm and Hygienic Responses to Fungal Pathogens
by Mark S. Bulmer, Bruno A. Franco and Edith G. Fields
Insects 2019, 10(8), 240; https://doi.org/10.3390/insects10080240 - 5 Aug 2019
Cited by 26 | Viewed by 5013
Abstract
In social insects, alerting nestmates to the presence of a pathogen should be critical for limiting its spread and initiating social mechanisms of defense. Here we show that subterranean termites use elevated vibratory alarm behavior to help prevent fatal fungal infections. The elevated [...] Read more.
In social insects, alerting nestmates to the presence of a pathogen should be critical for limiting its spread and initiating social mechanisms of defense. Here we show that subterranean termites use elevated vibratory alarm behavior to help prevent fatal fungal infections. The elevated alarm leads to elevated social hygiene. This requires that termites coalesce so that they can groom each other’s cuticular surfaces of contaminating conidial spores. Groups of 12 Reticulitermes flavipes workers varied in their response when immersed in conidia solutions of nine different strains of Metarhizium. Pathogen alarm displays of short 2–7-second bursts of rapid longitudinal oscillatory movement (LOM), observed over 12 min following a fungal challenge, were positively correlated with the time that workers spent aggregated together grooming each other. The frequency of these LOMs was inversely correlated with fatal fungal infections. The variation in fatalities appeared to be largely attributable to a differential response to Metarhizium brunneum and Metarhizium robertsii in the time spent in aggregations and the frequency of allogrooming. Isolated workers challenged with conidia did not display LOMs, which suggests that the alarm is a conditional social response. LOMs appear to help signal the presence of fungal pathogens whose virulence depends on the level of this emergency alert. Full article
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8 pages, 8062 KiB  
Communication
Foraging Macrotermes natalensis Fungus-Growing Termites Avoid a Mycopathogen but Not an Entomopathogen
by Kasun H. Bodawatta, Michael Poulsen and Nick Bos
Insects 2019, 10(7), 185; https://doi.org/10.3390/insects10070185 - 26 Jun 2019
Cited by 11 | Viewed by 5581
Abstract
Fungus-growing termites have to defend both themselves and their monoculture fungal cultivars from antagonistic microbes. One of the ways that pathogens can enter the termite colony is on the plant substrate that is collected by termite foragers. In order to understand whether foragers [...] Read more.
Fungus-growing termites have to defend both themselves and their monoculture fungal cultivars from antagonistic microbes. One of the ways that pathogens can enter the termite colony is on the plant substrate that is collected by termite foragers. In order to understand whether foragers avoid substrate infected with antagonists, we offered sub-colonies of Macrotermes natalensis a choice between food exposed to either a mycopathogenic or an entomopathogenic fungus, and control food. Workers did not show any preference between entomopathogen-exposed and control substrate, but significantly avoided the mycopathogen-exposed substrate. This suggests that the behaviour of foraging workers is more strongly influenced by pathogens affecting their crop than those posing risks to the termite workers themselves. Full article
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7 pages, 534 KiB  
Communication
Discovery of Aphid Lethal Paralysis Virus in Vespa velutina and Apis cerana in China
by Dahe Yang, Hongxia Zhao, Junming Shi, Xiang Xu, Yanyan Wu, Rui Guo, Dafu Chen, Xinling Wang, Shuai Deng, Sa Yang, Qingyun Diao and Chunsheng Hou
Insects 2019, 10(6), 157; https://doi.org/10.3390/insects10060157 - 3 Jun 2019
Cited by 13 | Viewed by 4755
Abstract
Honey bees are essential to the functioning of terrestrial ecosystems. However, despite no single factor being blamed for losses of honey bee colonies in Europe and the USA, viruses have been considered as a major driver. Moreover, a virus vector can enhance the [...] Read more.
Honey bees are essential to the functioning of terrestrial ecosystems. However, despite no single factor being blamed for losses of honey bee colonies in Europe and the USA, viruses have been considered as a major driver. Moreover, a virus vector can enhance the titer and virulence of virus such as Varroa destructor can change the virulence of the deformed wing virus. Here, we report molecular evidence for aphid lethal paralysis virus (ALPV) infecting Vespa velutina, which is an important predator of honey bees, especially of Apis cerana. Viral replication and phylogenetic analysis indicated that ALPV can not only replicate in V. velutina and A. cerana, but ALPV from A. cerana (ALPV-Ac) was also significantly associated with that of V. velutina (ALPV-Vv), though distinct from those of Apis mellifera (ALPV-Am). The host state posterior probability displayed that V. velutina is the main viral reservoir between V. velutina and A. cerana. Our results show ALPV had expanded host diversity resulting in potential impacts on the health of pollinators, even on the pollination ecosystem. We suggest further studies should investigate potential risks and impacts on pollinator populations of hornets. These results should have an impact conservation efforts focused on sustaining native pollinator abundance and diversity, and therefore, the crucial ecosystem services that they provide. Full article
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4 pages, 315 KiB  
Communication
Survival of Ectoparasitic Mites Tropilaelaps mercedesae in Association with Honeybee Hive Products
by Kitiphong Khongphinitbunjong, Panuwan Chantawannakul, Orlando Yañez and Peter Neumann
Insects 2019, 10(2), 36; https://doi.org/10.3390/insects10020036 - 29 Jan 2019
Cited by 2 | Viewed by 3250
Abstract
The global trade of honeybee hive products imposes the risk of the introduction of exotic pests. However, data on the potential of specific products enabling pest survival are often lacking. This holds especially true for ectoparasitic mites Tropilaelaps spp., which are mandatory pests [...] Read more.
The global trade of honeybee hive products imposes the risk of the introduction of exotic pests. However, data on the potential of specific products enabling pest survival are often lacking. This holds especially true for ectoparasitic mites Tropilaelaps spp., which are mandatory pests of honeybees in many countries. Here, we evaluated the longevity of Tropilaelaps mercedesae mites associated with empty honeycomb and dry pollen as two possible global import routes. Mites were able to survive up to three days in dry pollen and up to six days in empty honeycomb, thereby suggesting a sufficient time window for the potential introduction of T. mercedesae into mite-free countries via import of these hive products. Full article
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