P. Schmid-Hempel

Female mating frequencies in Bombus spp. from Central Europe.

Summary: The mating frequency of females in social insects is particularly interesting, because polyandry reduces colony relatedness and increases within-colony genetic variance. It thereby affects a complex balance of benefits and costs that determine the degree of reproductive skew, sex allocation to offspring, or the opportunities for nepotism and policing strategies. Few systematic surveys of female mating frequencies exist and many are based on unreliable behavioural observation or sperm counts. Here, we report the results of a survey of mating frequencies in eight European Bombus spp. by means of highly polymorphic microsatellite loci. Only B. hypnorum was found to be multiply mated, while the pattern found in B. terrestris, B. lucorum, B. pratorum, B. lapidarius, B. sicheli, B. hortorum, and B. pascuorum was compatible with single mating. The findings are compatible with recent claims that, with some exceptions, mating frequencies of social insect females are generally low.

Variation in genomic recombination rates among animal taxa and the case of social insects

Meiotic recombination is almost universal among sexually reproducing organisms. Because the process leads to the destruction of successful parental allele combinations and the creation of novel, untested genotypes for offspring, the evolutionary forces responsible for the origin and maintenance of this counter-intuitive process are still enigmatic. Here, we have used newly available genetic data to compare genome-wide recombination rates in a report on recombination rates among different taxa. In particular, we find that among the higher eukaryotes exceptionally high rates are found in social Hymenoptera. The high rates are compatible with current hypotheses suggesting that sociality in insects strongly selects for increased genotypic diversity in worker offspring to either meet the demands of a sophisticated caste system or to mitigate against the effects of parasitism. Our findings might stimulate more detailed research for the comparative study of recombination frequencies in taxa with different life histories or ecological settings and so help to understand the causes for the evolution and maintenance of this puzzling process.

Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites

Varroa-vectored virus pandemic Bees are facing several threats that are causing population collapses. Wilfert et al. found that European honey bees are the primary source of deformed wing virus (DWV) (see the Perspective by Villalobos). However, paradoxically, transmission between bees is inefficient. It seems that parasitic mites can facilitate virus transmission. European honeybees acquired the rapidly spreading Varroa mite from Asian honey bees, possibly via the commercial exchange of queens. Not only do bees suffer direct damage from the mites, but the bees are also efficiently inoculated with DWV. Science, this issue p. 594; see also p. 554 Pandemic virus infection in honeybees has been facilitated by the recent spread of a parasitic mite and by human trade. [Also see Perspective by Villalobos] Deformed wing virus (DWV) and its vector, the mite Varroa destructor, are a major threat to the world’s honeybees. Although the impact of Varroa on colony-level DWV epidemiology is evident, we have little understanding of wider DWV epidemiology and the role that Varroa has played in its global spread. A phylogeographic analysis shows that DWV is globally distributed in honeybees, having recently spread from a common source, the European honeybee Apis mellifera. DWV exhibits epidemic growth and transmission that is predominantly mediated by European and North American honeybee populations and driven by trade and movement of honeybee colonies. DWV is now an important reemerging pathogen of honeybees, which are undergoing a worldwide manmade epidemic fueled by the direct transmission route that the Varroa mite provides.

Mechanisms of pathogenesis and the evolution of parasite virulence

When studying how much a parasite harms its host, evolutionary biologists turn to the evolutionary theory of virulence. That theory has been successful in predicting how parasite virulence evolves in response to changes in epidemiological conditions of parasite transmission or to perturbations induced by drug treatments. The evolutionary theory of virulence is, however, nearly silent about the expected differences in virulence between different species of parasite. Why, for example, is anthrax so virulent, whereas closely related bacterial species cause little harm? The evolutionary theory might address such comparisons by analysing differences in tradeoffs between parasite fitness components: transmission as a measure of parasite fecundity, clearance as a measure of parasite lifespan and virulence as another measure that delimits parasite survival within a host. However, even crude quantitative estimates of such tradeoffs remain beyond reach in all but the most controlled of experimental conditions. Here, we argue that the great recent advances in the molecular study of pathogenesis provide a way forward. In light of those mechanistic studies, we analyse the relative sensitivity of tradeoffs between components of parasite fitness. We argue that pathogenic mechanisms that manipulate host immunity or escape from host defences have particularly high sensitivity to parasite fitness and thus dominate as causes of parasite virulence. The high sensitivity of immunomodulation and immune escape arise because those mechanisms affect parasite survival within the host, the most sensitive of fitness components. In our view, relating the sensitivity of pathogenic mechanisms to fitness components will provide a way to build a much richer and more general theory of parasite virulence.

Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi

Summary:Crithidia bombi is a prevalent endoparasite of bumblebees that is transmitted both horizontally between and vertically within colonies of its host, the bumble bee Bombus terrestris, and to the next generation. By experimentally infecting or not infecting laboratory-raised colonies with a standard inoculum before their transfer to the field, this study was aimed at evaluating the level of virulence of C. bombi under natural conditions. However, an unexpected finding was a substantial and seasonal increase in infections of natural populations, such that all colonies quickly became infected once exposed to the field. On average, experimentally infected colonies showed positive signs of infection 9.5 days after being exposed, not different from the 11.7 days in untreated colonies. Not surprisingly therefore, no significant differences between the two experimental groups in measures of colony success, such as male and young queen production or time of emergence of sexuals, were found. Overall though, C. bombi showed low levels of virulence which fits recent models for parasites with correlated horizontal and vertical transmission rates. On the other hand, the number of sexuals produced depended on the length of time over which reproduction could be sustained. Thus, early colonies and those with large first brood and large maximum size were at an advantage. Also, strong effects of site occurred. In addition, many colonies became naturally infected with the microsporidian Nosema bombi. Such infections were not associated with experimental treatment or colony size, but correlated with an increased production of sexuals, particularly males.

Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck

In early 1992, the European bumblebee, Bombus terrestris, was first seen in Tasmania and currently has spread to most of the island. Here, we report on the genetic structure, using micro-satellites, of the invading population from samples collected in the years 1998–2000, a few years after the first sighting of the species in its new area. The data show that the Tasmanian population has a very low genetic diversity, with less than half of the allelic richness (Richness=2.89 alleles; Hexp=0.591) and lower levels of heterozygosity as compared to populations in New Zealand (4.24 alleles; Hexp=0.729) and Europe (5.08 alleles; Hexp=0.826). In addition, the genetic data suggest that the invasion must have happened once, probably around late 1991, and was the result of very few, perhaps only two, individuals arriving in Tasmania. Furthermore, these founders came from the New Zealand population. Today, the population in the south of Tasmania seems to act as a source population from which individuals migrate into other parts of the state. A similar source–sink structure seems also the case for New Zealand. The data show that B. terrestris is a highly invasive species capable of establishing itself even after a dramatic genetic bottleneck. B. terrestris may be an invasive species due to the haplo–diploid sex determination system, which exposes recessive, deleterious mutations to selection. Offspring of such purged lines may then be able to tolerate high levels of inbreeding.

The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris.

This study reports the distribution of parasite genotypes for the trypanosome Crithidia bombi across individual units (the colonies) in host populations of a social insect, the bumble bee Bombus terrestris. A number of microsatellite primers were developed and several of them were found to be polymorphic in our samples. Furthermore, a simple algorithm was used to identify the likely multi-locus genotypes present in multiply infected host individuals. The results demonstrated a remarkably high degree of genetic diversity among infections. A first sample from 1997 could only use a low resolution with 2 loci and showed a total of 11 different genotypes of C. bombi from 12 colonies. The sample from 2000 was analysed at 6 polymorphic loci and contained data from 8 colonies that were infected by 27 different C. bombi genotypes. Roughly 16% of all individual bees but half of all colonies (2000 sample) were infected with more than 1 genotype. The infections in the different colonies were also genetically distinct from each other, and the parasite population as a whole was in linkage disequilibrium and deviated from Hardy-Weinberg expectations. The highly structured and genetically diversified population of C. bombi is likely to result from strong genotypic host-parasite interactions.

The population genetic structure of a large temperate pollinator species, Bombus pascuorum (Scopoli) (Hymenoptera: Apidae)

The genetic population structure of the bumble bee Bombus pascuorum was studied using six microsatellite loci and a partial sequence of the mitochondrial gene cytochrome b. Eighteen populations from central and northern Europe were included in the analysis. Observed levels of genetic variability and heterozygosity were high. Estimates of population differentiation based on F‐ and Φ‐statistics revealed significant genetic differentiation among B. pascuorum populations and suggest that two partially isolated gene pools, separated by the Alps, do exist. The distribution of mtDNA haplotypes supports this view and presents direct evidence for gene flow across the Alps. Estimates of the number of migrants exchanged among populations north of the Alps suggest that historical events may have left a strong imprint on population structure.

Sperm length, sperm storage and mating system characteristics in bumblebees

Summary: Multiple insemination induces sperm competition and may select for longer, faster moving sperm in species where sperm is short-lived and egg fertilization takes place almost immediately after ejaculation. Here we report the first detailed analysis of sperm length in social insects with long-term storage of sperm, using three bumblebee species with different mating systems as models. We show that individual males produce only one size-class of sperm, but that sperm length is highly variable among brothers, among unrelated conspecific males, and among males of different species. Males of Bombus hypnorum, a species with multiple-mating queens, have longer sperm than males of B. terrestris and B. lucorum whose queens are single mated. Although the sample size on the species level was too small to perform a phylogenetic analysis, this finding supports the hypothesis that, all other things being equal, multiple mating may select for longer sperm. Sperm length was positively correlated with male body size in B. terrestris and possibly in B. hypnorum, but not in B. lucorum. The variance of sperm length within single B. terrestris males before mating was consistently higher than the variance of ejaculated sperm that was stored in a queens spermatheca. Both longer sperm and shorter sperm could be preferentially stored, depending on the colony in which the males and queens were born and raised. These results indicate that the genotype of males may affect sperm length and that cryptic female choice of sperm length may have a genetic component as well.

Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees.

Many parasites, including important species that affect humans and livestock, must survive the harsh environment of insect guts to complete their life-cycle. Hence, understanding how insects protect themselves against such parasites has immediate practical implications. Previously, such protection has been thought to consist mainly of mechanical structures and the action of lectins. However, recently it has become apparent that gut infections may interact with the host immune system in more complex ways. Here, using bumble bees, Bombus terrestris and their non-invasive gut trypanosome, Crithidia bombi, as a model system we investigated the effects of parasitic infection, host resources and the duration of infections on the host immune system. We found that infection doubled standing levels of immune defence in the haemolymph (the constitutive pro-phenoloxidase system), which is used as a first, general defence against parasites. However, physical separation of the parasite from the haemolymph suggests the presence of a messenger system between the gut and the genes that control the pro-phenoloxidase system. Surprisingly, we found no direct effect of host resource-stress or duration of the infection on the immune system. Our results suggest a novel and tactical response of insects to gut infections, demonstrating the complexity of such host-parasite systems.