Sophie E. F. Evison

The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies

Summary 1. Over a million commercially produced bumblebee colonies are imported annually on a global scale for the pollination of greenhouse crops. After importation, they interact with other pollinators, with an associated risk of any parasites they carry infecting and harming native bees. National and supranational regulations are designed to prevent this, and commercially produced bumblebee colonies are accordingly now often sold and imported as being parasite-free. 2. Here, we used molecular methods to examine the occurrence of parasites in bumblebee colonies that were commercially produced in 2011 and 2012 by three producers. We then used controlled experiments to determine whether any parasites present were infectious. 3. We found that 77% of the commercially produced bumblebee colonies from the three producers, which were imported on the basis of being free of parasites, in fact carried microbial parasites, with five different parasites being detected across the total sample of bumblebees and a further three in the pollen supplied with the colonies as food. 4. Our controlled experiments demonstrated that at least three of these parasites were infectious to bumblebees with significant negative effects on their health. Furthermore, we also found that at least four of the parasites carried by commercially produced bumblebees were infectious to honeybees, indicating that they pose a risk to other pollinators as well. 5. Synthesis and applications. The results demonstrate that commercially produced bumblebee colonies carry multiple, infectious parasites that pose a significant risk to other native and managed pollinators. More effective disease detection and management strategies are urgently needed to reduce the pathogen spillover threat from commercially produced bumblebees.

Pervasiveness of parasites in pollinators

Many pollinator populations are declining, with large economic and ecological implications. Parasites are known to be an important factor in the some of the population declines of honey bees and bumblebees, but little is known about the parasites afflicting most other pollinators, or the extent of interspecific transmission or vectoring of parasites. Here we carry out a preliminary screening of pollinators (honey bees, five species of bumblebee, three species of wasp, four species of hoverfly and three genera of other bees) in the UK for parasites. We used molecular methods to screen for six honey bee viruses, Ascosphaera fungi, Microsporidia, and Wolbachia intracellular bacteria. We aimed simply to detect the presence of the parasites, encompassing vectoring as well as actual infections. Many pollinators of all types were positive for Ascosphaera fungi, while Microsporidia were rarer, being most frequently found in bumblebees. We also detected that most pollinators were positive for Wolbachia, most probably indicating infection with this intracellular symbiont, and raising the possibility that it may be an important factor in influencing host sex ratios or fitness in a diversity of pollinators. Importantly, we found that about a third of bumblebees (Bombus pascuorum and Bombus terrestris) and a third of wasps (Vespula vulgaris), as well as all honey bees, were positive for deformed wing virus, but that this virus was not present in other pollinators. Deformed wing virus therefore does not appear to be a general parasite of pollinators, but does interact significantly with at least three species of bumblebee and wasp. Further work is needed to establish the identity of some of the parasites, their spatiotemporal variation, and whether they are infecting the various pollinator species or being vectored. However, these results provide a first insight into the diversity, and potential exchange, of parasites in pollinator communities.

Genetic caste polymorphism and the evolution of polyandry in Atta leaf-cutting ants

Multiple mating by females with different males (polyandry) is difficult to explain in many taxa because it carries significant costs to females, yet benefits are often hard to identify. Polyandry is a derived trait in social insects, the evolutionary origins of which remain unclear. One of several leading hypotheses for its evolution is that it improves division of labour by increasing intra-colonial genetic diversity. Division of labour is a key player in the ecological success of social insects, and in many successful species of ants is based on morphologically distinct castes of workers, each with their own task specialisations. Atta leaf-cutting ants exhibit one of the most extreme and complicated forms of morphologically specialised worker castes and have been reported to be polyandrous but with relatively low mating frequencies (~2.5 on average). Here, we show for the first time that there is a significant genetic influence on worker size in Atta colombica leaf-cutting ants. We also provide the first estimate of the mating frequency of Atta cephalotes (four matings) and, by analysing much higher within-colony sample sizes, find that Atta are more polyandrous than previously thought (approximately six to seven matings). The results show that high polyandry and a genetic influence on worker caste are present in both genera of leaf-cutting ants and add weight to the hypothesis that division of labour is a potential driver of the evolution of polyandry in this clade of ants.

The cost of promiscuity: sexual transmission of Nosema microsporidian parasites in polyandrous honey bees.

Multiple mating (and insemination) by females with different males, polyandry, is widespread across animals, due to material and/or genetic benefits for females. It reaches particularly high levels in some social insects, in which queens can produce significantly fitter colonies by being polyandrous. It is therefore a paradox that two thirds of eusocial hymenopteran insects appear to be exclusively monandrous, in spite of the fitness benefits that polyandry could provide. One possible cost of polyandry could be sexually transmitted parasites, but evidence for these in social insects is extremely limited. Here we show that two different species of Nosema microsporidian parasites can transmit sexually in the honey bee Apis mellifera. Honey bee males that are infected by the parasite have Nosema spores in their semen, and queens artificially inseminated with either Nosema spores or the semen of Nosema-infected males became infected by the parasite. The emergent and more virulent N. ceranae achieved much higher rates of infection following insemination than did N. apis. The results provide the first quantitative evidence of a sexually transmitted disease (STD) in social insects, indicating that STDs may represent a potential cost of polyandry in social insects.

Host–parasite genotypic interactions in the honey bee: the dynamics of diversity

Parasites are thought to be a major driving force shaping genetic variation in their host, and are suggested to be a significant reason for the maintenance of sexual reproduction. A leading hypothesis for the occurrence of multiple mating (polyandry) in social insects is that the genetic diversity generated within-colonies through this behavior promotes disease resistance. This benefit is likely to be particularly significant when colonies are exposed to multiple species and strains of parasites, but host–parasite genotypic interactions in social insects are little known. We investigated this using honey bees, which are naturally polyandrous and consequently produce genetically diverse colonies containing multiple genotypes (patrilines), and which are also known to host multiple strains of various parasite species. We found that host genotypes differed significantly in their resistance to different strains of the obligate fungal parasite that causes chalkbrood disease, while genotypic variation in resistance to the facultative fungal parasite that causes stonebrood disease was less pronounced. Our results show that genetic variation in disease resistance depends in part on the parasite genotype, as well as species, with the latter most likely relating to differences in parasite life history and host–parasite coevolution. Our results suggest that the selection pressure from genetically diverse parasites might be an important driving force in the evolution of polyandry, a mechanism that generates significant genetic diversity in social insects.

Chemical Signature and Reproductive Status in the Facultatively Polygynous ant Pachycondyla Verenae

In insects, cuticular hydrocarbons (CHCs) generally are used as cues and signals for within colony processes, such as signaling reproductive status, and between colony processes, such as colony membership. We examined CHC profiles of the facultatively polygynous ant Pachycondyla verenae in order to identify chemical signals of reproductive queens within colonies containing many gynes. Colonies of P. verenae, belonging to two different members of a complex of morphospecies, were collected from three geographic localities within South America. We also tested whether CHC profiles differed between geographic localities and morphospecies. We found three alkenes, two isomers of pentacosene and heptacosene, which were more abundant in CHC profiles of reproductive queens of this morphospecies complex. When we tested whether these differences were consistent across geographic localities, we found the abundance of these alkenes differed according to morphospecies, with the isomers of pentacosene being more abundant in queens from morph one, and heptacosene being more abundant in queens from morph two. Our study has given further insight into the mechanisms behind maintenance of reproductive dominance, and has demonstrated that chemical signatures associated with reproductive status in Pachycondyla verenae are not conserved within this species complex.

Genetic diversity, virulence and fitness evolution in an obligate fungal parasite of bees

Within‐host competition is predicted to drive the evolution of virulence in parasites, but the precise outcomes of such interactions are often unpredictable due to many factors including the biology of the host and the parasite, stochastic events and co‐evolutionary interactions. Here, we use a serial passage experiment (SPE) with three strains of a heterothallic fungal parasite (Ascosphaera apis) of the Honey bee (Apis mellifera) to assess how evolving under increasing competitive pressure affects parasite virulence and fitness evolution. The results show an increase in virulence after successive generations of selection and consequently faster production of spores. This faster sporulation, however, did not translate into more spores being produced during this longer window of sporulation; rather, it appeared to induce a loss of fitness in terms of total spore production. There was no evidence to suggest that a greater diversity of competing strains was a driver of this increased virulence and subsequent fitness cost, but rather that strain‐specific competitive interactions influenced the evolutionary outcomes of mixed infections. It is possible that the parasite may have evolved to avoid competition with multiple strains because of its heterothallic mode of reproduction, which highlights the importance of understanding parasite biology when predicting disease dynamics.