Endoparasitic flies,pollen-collection by bumblebees and a potential host-parasite conflict

Summary Conopid flies (Conopidae, Diptera) are common larval parasites of bumblebees. The larva develops inside the abdomen of workers, queens and males. Development is completed within 10–12 days after oviposition when the host is killed and the parasite pupates in situ. Development results in parasitised bees becoming unable to carry large loads of nectar, as the conopid larvae reside where the honey crop is normally located. Furthermore, an addition to the bee's unloaden body mass is likely (average larval weight reached at pupation by the common parasite species Sicus ferrugineus: ±SD 36.3±12.3 mg, n=59; by Physocephala rufipes: 55.8±16.9 mg, n=108). We here asked whether the propensity of workers of the bumblebee Bombus pascuorum to collect nectar rather than pollen is related to the presence of conopid larvae. For samples of bees (n=2254 workers) collected over 3 years of field studies in northwestern Switzerland, there was no difference in the frequency of bees caught as pollen collectors among parasitised (38.1% of cases, n=210) as compared to non-parastised bees (43.9%, n=360) ( ²=1.83, n.s.). However, compared to the non-parasitised bees (n=360), those hosts containing a third (last) instar larva (n=9) were less likely to collect pollen than expected by chance ²=6.91, P=0.003. Similarly, hosts with short survival time between capture and being killed by the developing larva (which hence must have harboured a late instar parasite at time of capture) were less likely to collect pollen (8%, n=25) than those found not parasitised (37.6%, n=891 ²=9.16, P<0.001). Late instar larvae grow so big that they fill the entire abdomen. Although there was also a tendency for presumably older bees to collect less pollen, this is unlikely to explain the observations. We also discuss whether these changes in foraging behaviour of bumblebees may reflect a host-parasite conflict over the type of resource to be collected.     

The evolution of female multiple mating in social hymenoptera

Abstract The evolution of female multiple mating is a highly controversial topic, especially in social insects. Here we analyze, using comparative analyses and simulation models, the merits of two major contending hypotheses for the adaptive value of polyandry in this group. The hypotheses maintain that, respectively, the resulting genotypic diversity among offspring within a colony: (1) mitigates against the effects of parasites; or (2) favors adaptive division of labor. Only two of 11 phylogenetically uncontrolled comparative analyses supported an association between polyandry and the complexity of division of labor (measured here using worker caste polymorphism or polyethism) as proposed by hypothesis 2, and after controlling for phylogeny there were no significant associations. In contrast, a previous study demonstrated such an association for parasite load as expected under hypothesis 1. In addition, we used simulation models to track the spread of an initially rare allele for double mating in a population of single-mating alleles, thus analyzing the crucial first step from monandry to polyandry. We find that double mating evolves consistently under antagonistic coevolution given that parasites exert sufficient selection intensity. In contrast, selection for enhanced division of labor resulted in only an erratic appearance of polyandry in highly (and mostly negatively) autocorrelated environments where no coevolutionary dynamics were allowed. Together, we interpret these results to suggest that parasites, and the antagonistic coevolutionary pressures they exert, may play an important role in the evolution of polyandry in social hymenopteran populations.     

Low parasite loads accompany the invading population of the bumblebee, Bombus terrestris in Tasmania

In its native Europe, the bumblebee, Bombus terrestris (L.) has co-evolved with a large array of parasites whose numbers are negatively linked to the genetic diversity of the colony. In Tasmania B. terrestris was first detected in 1992 and has since spread over much of the state. In order to understand the bee’s invasive success and as part of a wider study into the genetic diversity of bumblebees across Tasmania, we screened bees for co-invasions of ectoparasitic and endoparasitic mites, nematodes and micro-organisms, and searched their nests for brood parasites. The only bee parasite detected was the relatively benign acarid mite Kuzinia laevis (Dujardin) whose numbers per bee did not vary according to region. Nests supported no brood parasites, but did contain the pollen-feeding life stages of K. laevis. Upon summer-autumn collected drones and queens, mites were present on over 80% of bees, averaged ca. 350–400 per bee and were more abundant on younger bees. Nest searching spring queens had similar mite numbers to those collected in summer-autumn but mite numbers dropped significantly once spring queens began foraging for pollen. The average number of mites per queen bee was over 30 fold greater than that reported in Europe. Mite incidence and mite numbers were significantly lower on worker bees than drones or queens, being present on just 51% of bees and averaging 38 mites per bee. Our reported incidence of worker bee parasitism by this mite is 5–50 times higher than reported in Europe. That only one parasite species co-invaded Tasmania supports the notion that a small number of queens founded the Tasmanian population. However, it is clearly evident that both the bee in the absence of parasites, and the mite have been extraordinarily successful invaders. Received 12 April 2006; revised 10 November 2006; accepted 15 November 2006.     

Strain filtering and transmission of a mixed infection in a social insect

Mixed-genotype infections have attracted considerable attention as drivers of pathogen evolution. However, experimental approaches often overlook essential features of natural host-parasite interactions, such as host heterogeneity, or the effects of between-host selection during transmission. Here, following inoculation of a mixed infection, we analyse the success of different strains of a trypanosome parasite throughout the colony cycle of its bumblebee host. We find that most colonies efficiently filter the circulating infection before it reaches the new queens, the only offspring that carry infections to the next season. A few colonies with a poor filtering ability thus contributed disproportionately to the parasite population in the next season. High strain diversity but not high infection intensity within colony was associated with an increased probability of transmission of the infection to new queens. Interestingly, the representation of the different strains changed dramatically over time, so that long-term parasite success could not be predicted from short-term observations. These findings highlight the shaping of within-colony parasite diversity through filtering as a crucial determinant of year-to-year pathogen transmission and emphasize the importance of host ecology and heterogeneity for disease dynamics.     

In vivo dynamics of an immune response in the bumble bee Bombus terrestris

Concepts from evolutionary ecology have recently been applied to questions of immune defences. However, an important but often neglected aspect is the temporal dynamics of the simple immune measures used in ecological studies. Here, we present observations for workers of the bumble bee Bombus terrestris on the dynamics of the phenoloxidase (PO) system, antibacterial activity, and the total number of haemocytes following a challenge with immune elicitors (LPS, Laminarin), over a time-span ranging from 1min to 14 days. The dynamics of the PO measurement showed a complex pattern and was correlated with haemocyte counts. Antibacterial activity, on the other hand, increased sharply between 2 and 24h post-challenge followed by a slow decrease. Surprisingly, the effects of a challenge lasted up to 14 days.     

Heritability of sperm length in the bumblebee Bombus terrestris

Sperm length is highly variable, both between and within species, but the evolutionary significance of this variation is poorly understood. Sexual selection on sperm length requires a significant additive genetic variance, but few studies have actually measured this. Here we present the first estimates of narrow sense heritability of sperm length in a social insect, the bumblebee Bombus terrestris. In spite of a balanced and straightforward rearing design of colonies, and the possibility to replicate measurements of sperm within single males nested within colonies, the analysis proved to be complex. Several appropriate statistical models were derived, each depending on different assumptions. The heritability estimates obtained ranged from h ² = 0.197 ± 0.091 to h ² = 0.429 ± 0.154. All our estimates were substantially lower than previous estimates of sperm length heritability in non-social insects and vertebrates.     

Antagonistic Coevolution Accelerates the Evolution of Reproductive Isolation in Tribolium castaneum

Abstract The evolution of reproductive isolation among populations is often the result of selective forces. Among those, parasites exert strong selection on host populations and can thus also potentially drive reproductive isolation. This hypothesis has yet to be explicitly tested, and here we set up a multigenerational coevolution experiment to explore this possibility. Five lines of Tribolium castaneum were allowed to coevolve with their natural parasite, Nosema whitei; five paired lines of identical origin were maintained in the absence of parasites. After 17 generations, we measured resistance within and reproductive isolation between all lines. Host lines from the coevolution treatment had considerably higher levels of resistance against N. whitei than their paired host lines, which were maintained in the absence of parasites. Reproductive isolation was greater in the coevolved selection regime and correlated with phenotypic differentiation in parasite resistance between coevolved host lines. This suggests the presence of a selection-driven genetic correlation between offspring number and resistance. Our results show that parasites can be a driving force in the evolution of reproductive isolation and thus potentially speciation.     

A field study on the influence of food and immune priming on a bumblebee–gut parasite system

Laboratory experiments are often preferred over field experiments because they allow the control of confounding factors that would otherwise influence the causal effect of a particular focal experimental factor. These confounding factors can, however, significantly alter the response of an organism confronted with a particular situation, which can have great implications. In a field experiment with a bumblebee host–parasite system, we looked at the influence of additional food supply and immune challenge on various colony fitness values and parasite traits. We could confirm the importance of food on the colony fitness, but not on parasite infection probability or parasite genetic diversity. In contrast to the findings of laboratory experiments of this system, challenge of the immune system had no significant effect on colony fitness or parasite infections. These results likely reflect an overriding effect of environmental variation without disproving the concept of a cost of defence per se. But the results also demonstrate that confounding factors purposely controlled for in the laboratory have to be weighed against their ecological relevance, and stress the need for careful analysis before any direct transfer is made of laboratory results to field situations.     

Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system

Specific interactions between parasite genotypes and host genotypes (G_p × G_h) are commonly found in invertebrate systems, but are largely lacking a mechanistic explanation. The genotype of invertebrate hosts can be complemented by the genomes of microorganisms living on or within the host (‘microbiota’). We investigated whether the bacterial gut microbiota of bumble bees (Bombus terrestris) can account for the specificity of interactions between individuals from different colonies (previously taken as host genotype proxy) and genotypes of the parasite Crithidia bombi. For this, we transplanted the microbiota between individuals of six colonies. Both the general infection load and the specific success of different C. bombi genotypes were mostly driven by the microbiota, rather than by worker genotype. Variation in gut microbiota can therefore be responsible for specific immune phenotypes and the evolution of gut parasites may be driven by interactions with ‘microbiota types’ as well as with host genotypes.