Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies

October 28, 2015

From: The ISME Journal | Multidisciplinary Journal of Microbial Ecology

Gideon J Mordecai1,2, Laura E Brettell3, Stephen J Martin3, David Dixon1, Ian M Jones2 and Declan C Schroeder1


Over the past 50 years, many millions of European honey bee (Apis mellifera) colonies have died as the ectoparasitic mite, Varroa destructor, has spread around the world. Subsequent studies have indicated that the mite’s association with a group of RNA viral pathogens (Deformed Wing Virus, DWV) correlates with colony death. Here, we propose a phenomenon known as superinfection exclusion that provides an explanation of how certain A. mellifera populations have survived, despite Varroa infestation and high DWV loads. Next-generation sequencing has shown that a non-lethal DWV variant ‘type B’ has become established in these colonies and that the lethal ‘type A’ DWV variant fails to persist in the bee population. We propose that this novel stable host-pathogen relationship prevents the accumulation of lethal variants, suggesting that this interaction could be exploited for the development of an effective treatment that minimises colony losses in the future.



The recent global decline of the European honey bee (Apis mellifera) populations (Ratnieks and Carreck, 2010; Schroeder and Martin, 2012) is of grave concern because of their role as pollinators which contribute an estimated $225 billion to the global economy (Gallai et al., 2009). For over half a century, the global spread of the ectoparasitic mite, Varroa destructor, has resulted in the death of many millions of managed and feral honey bee colonies (Martin et al., 2012; Schroeder and Martin, 2012; Thompson et al., 2014). The mite has introduced a new viral transmission route that has dramatically altered the viral landscape (Martin et al., 2012). This has resulted in a massive loss of diversity in Deformed Wing Virus (DWV) (Martin et al., 2012), the pathogen now linked with the collapse of honey bee colonies (Highfield et al., 2009; Di Prisco et al., 2011). However, prior to Varroa spread, DWV stably co-existed with honey bees (Martin et al., 2012) albeit at viral loads many orders of magnitude lower than is now observed (Martin et al., 2012; Mondet et al., 2014). For example, the recent arrival of Varroa into the Hawaiian honey bee population was accompanied by a million fold increase in the viral load of DWV, loss of DWV diversity and the predominance of a single highly virulent DWV variant (type A) (Martin et al., 2012). These landscape scale changes have also been demonstrated at the individual honey bee level within the UK honey bee population. For example, Ryabov et al. (2014) demonstrated the dominance of a single variant of DWV when a mixture of viral strains were injected into developing pupae leading to a rapid loss of DWV diversity and million fold increase in viral loads.


In the early 1990s, Varroa swept across the UK and was followed by widespread colony deaths 1–3 years later. To ensure the long-term survival of their honey bee colonies, beekeepers in Varroa-infested countries manage Varroa populations (Sumpter and Martin, 2004), largely through chemical methods. Nonetheless, there are reports of rare isolated untreated A. mellifera colonies of European origin thriving despite Varroa infestation, including cases on an island in Brazil (DeJong and Soares, 1997) and in small forest patches in France (Conte et al., 2007) and New York, USA (Seeley, 2007). The survival of these colonies is well documented and not questioned, however, the mechanism by which tolerance to Varroa and its association with DWV is maintained remains elusive. In the UK, a small number of beekeepers opted not to control their mite populations and, in most cases, lost their bees. However, one UK beekeeper, Ron Hoskins, initiated a closed breeding programme from colonies that survived the initial Varroa infestation and this isolated population of up to 40 colonies persists in Swindon, central England, without chemical control of Varroa ( The aim of this study was to assess the viral landscape in this apiary thereby determining whether the colonies remained disease-free owing to an absence of DWV. We show here that the Swindon apiary is dominated by an avirulent DWV type B master variant with the concomitant absence of the virulent DWV type A master variant. Taken together, these data suggest that a phenomenon known as superinfection exclusion (SIE) (Salaman, 1933; Labrie et al., 2010) is a plausible explanation for why this isolated UK honey bee population has survived, despite Varroa infestation and high DWV loads.

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