Viral drivers of honey bee losses the DWV-clade and the AKI-complex

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1 Viral drivers of honey bee losses the DWV-clade and the AKI-complex Marc Oliver Schäfer OIE Symposium on Emerging Infectious Agents in Honey Bees & OIE-Listed diseases

2 Honey bee colony losses Estimated annual honey bee colony mortality in Europe EPILOBEE 2012/13 EPILOBEE 2013/14 Mayor drivers of losses (Jacques et al. 2017): Beekeeper background and apicultural practices Colony mortality rates [%] in all participating Member States of the European Union, recorded throughout the EPILOBEE study European Commission, ANSES, EURL (modified)

3 Honey bee colony losses Estimated honey bee colony mortality in the US The top five reasons (vanengelsdorp Estimated et al. percentage 2012): of Starvation colonies lost due to each Weak colonies in the fall commonly self-reported Poor wintering conditions colony health risk factors Poor queens in season Varroa mites (Kulhanek et al. 2017). Kulhanek et al beeinformed.org Summary of total overwintering colony losses in the US (The acceptable winter loss rate shows the average of acceptable yearly colony losses declared by survey participants in each year)

4 Mortality [%] Honey bee colony losses Estimated honey bee overwintering colony mortality in Germany The identified factors involved (Genersch et al. 2010): High V. destructor infestation levels Clinically relevant DWV infections in autumn ABPV infections in autumn Old queens Relative colony weakness before overwintering / / / / / / / / / / / / /17 written survey "MAYEN" monitored colonies "DeBiMo" all colonies "DeBiMo" "EPILOBEE" Surveyed winter Results of the German bee monitoring project ( DeBiMo ) in comparison with a written survey ( MAYEN = passive surveillance) and the results of the pan- European epidemiological study EPILOBEE

5 Factors that influence honey bee health Pesticides claudiaspahr.com Weather / climate Vitality & diversity of the honey bees Beekeeping practice Kathy Keatley Garvey Diseases of the honey bee ALP Ritter Quantity & quality of the nutrition Zach Huang Fries

6 Diseases of the honey bee Viruses (e.g. DWV, SBV) Bacteria (e.g. Foulbrood) Parasitoids (e.g. A. borealis) Rosenkranz USDR-ARS Ritter PlosOne Fungi (e.g. Chalkbrood) Ectoparasites (e.g. Varroa & Tropilaelaps spp.) Aronstein Other pests (e.g. Aethina tumida & V. velutina) Endoparasites (e.g. Nosema apis & N. ceranae) Zach Huang Jean Haxaire Fries

7 Viruses associated with honey bees The AKI-complex The DWV-clade Francis 2012 Francis 2012

8 AKI-complex world distribution West African Republic of Benin (Amakpe et al. 2015) Argentina (Molineri et al. 2017) Elsevier / Journal of Invertebrate Pathology 103, de Miranda et al (modified)

9 DWV world distribution Science 351, /science.aac9976, Wilfert et al (modified) IBRA / Bee World 86, Ellis and Munn 2005 Wilfert et al. (2016) have shown that DWV is globally distributed, (A) driven by trade and movement of honey bee colonies, and (B) is following the spread-pattern of V. destructor However, a recent study showed the absence of DWV in Australia (Roberts et al. 2017) Science 351, /science.aac9976, Wilfert et al (modified) Roberts JMK, Anderson DL and Durr PA 2017

10 Transmission of viruses in honey bees Gudrun Koeniger Elsevier / Journal of Invertebrate Pathology 92, Chen et al (modified)

11 Transmission of viruses through Varroa destructor Varroa destructor is transmitting several viruses: o DWV (Bowen-Walker et al. 1999) o ABPV (Ball 1983) o KBV (Chen et al. 2004, Shen et al. 2005) o IAPV (de Prisco et al. 2011) Varroa destructor is a biological vector for DWV (Ongus et al. 2004, Yue and Genersch 2005) egg 1 Protonymph Deutonymph egg 2 egg 3 egg 4 egg 5 Adult male Adult female mating Mother mite with two daughter mites leaving the worker brood cell Elsevier / Journal of Invertebrate Pathology 103, Rosenkranz et al (modified)

12 Transmission of viruses through Varroa destructor BQCV CBPV SBV Other? viruses AKI-complex DWV-clade + Varroa destructor Elsevier / Current Opinion in Insect Science 8, McMenamin and Genersch 2015 (modified)

13 Clinical symptoms of paralysis Photos courtesy of The Animal and Plant Health Agency (APHA), Crown Copyright Death of lethally infected bees is preceded by a rapidly progressing paralysis, including trembling, inability to fly and the gradual darkening and loss of hair from the thorax and abdomen (ABPV & IAPV), symptoms usually associated with CBPV. Severe ABPV & KBV infection causes a sharp decline in the adult bee population.

14 Clinical symptoms of IAPV infection PLoS ONE 8(9): e73429; Boncristiani et al. 2013

15 Clinical symptoms of DWV infection Rosenkranz ALP Pupal death emergence of non-viable, malformed bees discolouring healthy looking bees suffering from ataxia and disorientation (Yang and Cox-Foster 2007). Such bees are non-viable and die within 67 hours after emerging (Möckel et al. 2011).

16 Viruses and Varroa destructor Hawaii 2009 = Varroa free = Varroa infested Rosenkranz Viral load, prevalence and genetic diversity of DWV across the four main islands that have been exposed to Varroa destructor for different periods of time Science 336, /science , Martin et al (modified) DWV has changed dramatically in prevalence, load and strain diversity after the new arrival of V. destructor into former mite-free honey bee populations in Hawaii

17 Viruses and Varroa destructor Roberts JMK, Anderson DL and Durr PA 2017

18 V. destructor per 100 bees [%] Viruses and Varroa destructor Results of the German bee monitoring (data from ) show that the higher the colony infestation level with V. destructor, the higher is the chance of infections with ABPV and/or DWV N= N= N=2.540 B* C* 5 A* 0 kein no DWV ABPV/DWV / kein ABPV DWV ABPV oder or DWV ABPV ABPV DWV und and ABPV DWV * Different letters indicate a significant difference (H-Test (Kruskal-Wallis); P<0,001)

19 Overwintering mortality [%] Overwintering mortality [%] Viruses and colony losses If ABPV or DWV are detected in a colony in autumn, the higher is the chance that the colony will not survive the following winter 25 ABPV Colony nicht not im infected Volk gefunden with ABPV ABPV Colony im Volk infected gefunden with ABPV 25 DWV Colony nicht not im infected Volk gefunden with DWV DWV Colony im Volk infected gefunden with DWV N= N=3.288 * N= N=2.736 *** * Chi-Quadrat; P<0, *** Chi-Quadrat; P<0,0001

20 Viruses and colony losses CCD has resulted in a loss of 50 to 90% of colonies in affected beekeeping operations across the US IAPV was strongly correlated with CCD (Cox-Foster et al. 2007) SCIENCE / /science , Cox-Foster et al (modified) SCIENCE / /science , Cox-Foster et al (modified)

21 C o n s P r o s Honey bee virus diagnostic Enzyme-Linked ImmunoSorbent Assay (ELISA) ELISA is a complex multistep assay involving sensitive enzymatic reporters. There are many opportunities for assay failure. Polymerase Chain Reaction (PCR) is the most commonly used technique Gel-based detection Fluorescence-based detection Nested/semi-nested PCR classical PCR Real-time PCR without probes (intercalating dyes) Real-time PCR with probes (TaqMan, FRET, Beacon) Sensitive Sensitive and high specific Highly sensitive and specific moderate costs for consumables and PCR cycler Sensitive and specific moderate costs for consumables and PCR cycler Time-saving Reduced risk of crosscontaminations High-throughput analyses Time-saving minimal risk of crosscontaminations High-throughput analyses Semi-/quantitative results Semi-/quantitative results Time-consuming Qualitative results Very high risk of crosscontaminations Confirmation of specificity by fragment size Time-consuming Qualitative results High risk of crosscontaminations Confirmation of specificity by fragment size Confirmation of specificity by melting curve analysis Cost for real-time PCR cycler Reduced diagnostic sensitivity based on additional probe Cost for probes and realtime PCR cycler

22 Occurrence [%] Occurrence [%] Honey bee virus diagnostic ABPV BQCV CBPV DWV KBV SBV Varroa 0 ABPV BQCV CBPV DWV KBV SBV Varroa

23 Honey bee virus diagnostic European Communities, Virology and the Honey Bee, 2008 The most common bee viruses use their own RNA-dependent RNA polymerases to replicate. These enzymes lack the proof-reading capability seen in their DNA counterparts, and this leads to high error rates. The resulting genotypic variants give the virus a remarkable evolutionary rate and the mixed population of mutant viral genotypes is referred to as a quasispecies. For DWV it is already accepted that it exists as a quasispecies (Martin et al. 2012, Mordecai et al. 2016), that is also called the DWV-clade (de Miranda and Genersch 2010).

24 Honey bee virus diagnostic

25 DWV-clade diagnostic Conventional PCR targeting multiple regions of the DWV genome Real time TaqMan PCR Chen et al. 2005, Applied and Environmental Microbiology 71 (modified) Elsevier / The Veterinary Journal 169, Genersch 2005 (modified) Forsgren et al. 2009, Springer / Exp. Appl. Acarol. 47 (modified) Real time SYBR Green PCR targeting multiple regions of the DWV genome Elsevier / The Journal of Invertebrate Pathology 91, Chantawannakul et al (modified) With the use of (next-generation) sequencing the DWV quasispecies will be further investigated. Thus, Mordecai et al. (2016) have shown that the DWV species complex is made up of three master variants: DWV Type A, B and C McMahon et al. 2017, Proc. R. Soc. B 283, the Royal Society (modified)

26 AKI-complex diagnostic Real time SYBR Green PCR targeting multiple regions of the IAPV genome AKI Primers American Society for Microbiology / Journal of Virology 82, Palacios et al (modified) Real time TaqMan PCR PLoS ONE 7 e30641, Evison et al (modified) Francis and Kryger 2012, Journal of Apicultural Science 56 (modified) The design of primers that allow the detection of ABPV, KBV and IAPV in a single assay reduce cost & time. Only AKI-positive samples will be combined with specific PCRs. Elsevier / The Journal of Invertebrate Pathology 91, Chantawannakul et al (modified)

27 Conclusions Honey bee health is influenced by multiple factors, diseases play a major role Varroosis seems to be a main cause for worldwide honey bee colony losses Varroosis = infestation with V. destructor plus infection with viruses that are associated with the mite Viruses of the DWV clade and the AKI-complex are spread worldwide. Where there are bees, there are viruses Most of honey bee viruses are RNA-based and have a quasispecies nature. For DWV, its quasispecies nature is already accepted Detection of honey bee viruses is currently based on RT-PCR methods and new developments will improve future diagnostics The combination of clinical symptoms and the diagnosis of distinct virus-combinations and their titers may help explaining bee-losses

28 OIE-listed diseases of the honey bee Acarapisosis American foulbrood European foulbrood Forsgren Varroosis Tropilaelaps infestation Small hive beetle infestation

29 OIE-listed diseases of the honey bee Acarapisosis American foulbrood European foulbrood Varroosis and associated viruses ALP Tropilaelaps infestation Small hive beetle infestation Forsgren

30 Thank you! Dr. Marc Schäfer National Reference Laboratory for Bee Diseases Institut of Infectology (IMED) Friedrich-Loeffler-Institut FLI Federal Institute for Animal Health Südufer Greifswald - Insel Riems GERMANY; Tel:

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