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Biomedical subjects

P Schmid-Hempel

Publications and source records attributed to P Schmid-Hempel.

At least 19 recordsLinked to original sources

Selection by parasites may increase host recombination frequency.

Meiotic recombination destroys successful genotypes and it is therefore thought to evolve only under a very limited set of conditions. Here, we experimentally show that recombination rates across two linkage groups of the host, the red flour beetle Tribolium castaneum, increase with exposure to the microsporidian parasite, Nosema whitei, particularly when parasites were allowed to coevolve with their hosts. Selection by randomly varied parasites resulted in smaller effects, while directional selection for insecticide resistance initially reduced recombination slightly. These results, at least tentatively, suggest that short-term benefits of recombination--and thus the evolution of sex--may be related to parasitism.

Animals↗

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.

Adjuvants, Immunologic↗

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.

Algorithms↗

Effects of sperm on female longevity in the bumble-bee Bombus terrestris L.

The male ejaculate, particularly the accessory gland products, has been shown to affect female survival (as is best understood in Drosophila melanogaster). So far, these findings have primarily been discussed in the context of a sexual conflict and multiple mating. Here, we show that in the bumble-bee Bombus terrestris, male genotype influences female longevity even though B. terrestris generally is a singly mated species and male and female interests may thus be more convergent. In addition, the effect could not be owing to accessory gland products, as we artificially inseminated the queens with the content of the accessory testes only.

Analysis of Variance↗

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.

Animals↗

Queen-controlled sex ratios and worker reproduction in the bumble bee Bombus hypnorum, as revealed by microsatellites.

Social insect colonies provide model systems for the examination of conflicts among parties with different genetic interests. As such, they have provided the best tests of inclusive fitness theory. However, much remains unknown about in which party's favour such conflicts are resolved, partly as a result of the only recent advent of the molecular tools needed to examine the outcome of these conflicts. Two key conflicts in social insect colonies are over control of the reproductive sex ratio and the production of male offspring. Most studies have examined only one of these conflicts but in reality they occur in tandem and may influence each other. Using microsatellite analyses, the outcome of conflict over sex ratios and male production was examined in the bumble bee, Bombus hypnorum. The genotypes were determined for mother queens, their mates and males for each of 10 colonies. In contrast to other reports of mating frequency in this species, all of the queens were singly mated. The population sex ratio was consistent with queen control, suggesting that queens are winning this conflict. In contrast, workers produced over 20% of all males in queen-right colonies, suggesting that they are more effective in competing over male-production. Combining these results with previous work, it is suggested that worker reproduction is a labile trait that may well impose only small costs on queen fitness.

Alleles↗

Immune defence in bumble-bee offspring.

Immune-challenged vertebrate females transfer specific antibodies to their offspring, but this gratuitous immunity cannot operate in invertebrates. Here we show that constitutive immune defence is enhanced in sexual offspring of the bumble-bee Bombus terrestris L. when the parental colony is immune-challenged. Our findings indicate that invertebrates may use a different component of the immune system to generate a facultative trans-generational increase in the immune response.

Animals↗

Males of social insects can prevent queens from multiple mating.

During copulation, males of Bombus terrestris fill the queen's sexual tract with a mating plug after transferring their sperm. The sticky secretion is produced by the male's accessory glands and disappears within a couple of days. Experiments now show that the primary function of the plug is to reduce the subsequent mating probability of the queen. The plug is not efficient in preventing sperm migration into the spermatheca. Due to its low energetic value, the plug is also unlikely to serve as a nuptial gift. This type of male interference with female mating propensity has so far not been found in social insects. This finding could, at least tentatively, explain why females of B. terrestris may not be able to take advantage of the demonstrated benefits of multiple mating. Furthermore, such male interference could be a more general phenomenon in social insects, with obvious ramifications for the evolution of polyandry in this group.

Animals↗

A nonspecific fatty acid within the bumblebee mating plug prevents females from remating.

The best mating strategy for males differs from that of females, because females gain from mating with several males (polyandry), but males gain from monopolizing the females. As a consequence, males have evolved a variety of methods, such as the transfer of inhibitory substances from their accessory glands, to ensure exclusive paternity of the female's offspring, generally with detrimental effects on female fitness. Inhibitory substances have been identified as peptides or other specific molecules. Unfortunately, in social insects male-mating traits are investigated only poorly, although male social insects might have the same fundamental influence on female-mating behavior as found in other species. A recently developed technique for the artificial insemination of bumblebee queens allowed us to investigate which chemical compound in the mating plug of male bumblebees, Bombus terrestris L., prevents females (queens) from further mating. Surprisingly, we found that the active substance is linoleic acid, a ubiquitous and rather unspecific fatty acid. Contrary to mating plugs in other insect species, the bumblebee mating plug is highly efficient and allows the males to determine queen-mating frequencies.

Animals↗

On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites.

Over the last decade, there has been a major shift in the study of adaptive patterns and processes towards including the role of host-parasite interactions, informed by concepts from evolutionary ecology. As a consequence, a number of major questions have emerged. For example, how genetics affects host-parasite interactions, whether parasitism selects for offspring diversification, whether parasite virulence is an adaptive trait, and what constrains the use of the host's immune defences. Using bumblebees, Bombus spp, and their parasites as a model system, answers to some of these questions have been found, while at the same time the complexity of the interaction has led expectations away from simple theoretical models. In addition, the results have also led to the unexpected discovery of novel phenomena concerning, for instance, female mating strategies.

Animals↗

A linkage analysis of sex determination in Bombus terrestris (L.) (Hymenoptera: Apidae).

We constructed a linkage map of Bombus terrestris (Hymenoptera, Apidae) phase unknown. The map contains 79 markers (six microsatellite and 73 RAPD markers) in 21 linkage groups and spans over 953.1 cM. The minimal recombinational size of the B. terrestris genome was estimated to be 1073 cM. Using flow cytometry, the physical size of the haploid genome of B. terrestris was calculated to be 274 Mb. This is the second linkage map for a social insect species. Bombus terrestris has on average five times less recombinational events per kb than the honey bee Apis mellifera. Male haploidy, chromosome size, and eusociality can now be excluded as reasons for the high recombination frequency of Apis mellifera. Finally, the sex determination locus of B. terrestris was placed on the map using bulked segregant analysis.

Animals↗

Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris.

Multiple mating by females (polyandry) is taxonomically widespread but the evolution of such behaviors is not clearly understood given potential costs of polyandry such as time, energy, or predation risk. The genetic variability versus parasites hypothesis predicts a reduction of parasitism due to increased genetic variability among offspring and an associated fitness gain. We tested this hypothesis with a field experiment in the bumblebee, Bombus terrestris L. Worker heterogeneity within the colony was experimentally altered by artificially inseminating queens with sperm from one male, four brothers, two males, or four unrelated males. We found genetic variability to be effective, because intensity and prevalence of the most common parasite, Crithidia bombi, a trypanosome, decreased with increasing levels of colony heterogeneity. Fitness differed between treatments but did not increase in a simple way, with increasing genetic heterogeneity among colony workers. Instead, fitness followed a U-shaped function with a minimum for small amounts of genetic heterogeneity. We therefore suggest that polyandry also induces a cost, perhaps as a result of the social structure within the colony. In evolutionary terms, singly mated females appear to be constrained by an adaptive valley that needs to be crossed before high degrees of mating frequency can be reached. This may help to explain why B. terrestris and most other social insects are often monandrous.

Animals↗

Survival for immunity: the price of immune system activation for bumblebee workers.

Parasites do not always harm their hosts because the immune system keeps an infection at bay. Ironically, the cost of using immune defenses could itself reduce host fitness. This indirect cost of parasitism is often not visible because of compensatory resource intake. Here, workers of the bumblebee, Bombus terrestris, were challenged with lipopolysaccharides and micro-latex beads to induce their immune system under starvation (i.e., not allowing compensatory intake). Compared with controls, survival of induced workers was significantly reduced (by 50 to 70%).

Animals↗

Phylogenetic relationships among bumble bees (Bombus, latreille) inferred from mitochondrial cytochrome b and cytochrome oxidase I sequences.

We conducted a molecular study intending to derive an estimate of the relationships within the genus Bombus (bumble bees) by comparing the mitochondrial cytochrome b and cytochrome oxidase I (COI) genes from 19 species, spanning 10 of approximately 16 European subgenera and 3 subgenera from North and South America. Our trees differ from the most recent classifications of bumble bees. Although bootstrap values for deep branches are low, our sequences show significant data structure and low homoplasy, and all trees share some groups and patterns. In all cases, the subgenus Bombus s. str. clusters among the most derived bumble bees, contrary to other molecular studies. In all trees, B. funebris is the sister taxon of B. robustus, and in five of the six trees, B. wurflenii is the sister taxon to this clade. B. nevadensis is basal to the other species in the analysis of the cytochrome b gene, but appears to be among the most derived according to the analysis of the COI region. The species representing the subgenera Thoracobombus and Fervidobombus are consistently among the earliest diverged. Species that appear in very different positions in different trees are B. nevadensis, B. mesomelas, B. balteatus, and B. hyperboreus. All subgenera with two representatives in our analysis are apparently monophyletic except Fervidobombus, Melanobombus, and Pyrobombus. The groups formed by pocket makers and non-pocket makers within Bombus also appear to be paraphyletic, and therefore some subgenera may not accurately reflect phylogeny.

Animals↗

Mating, parasites and other trials of life in social insects.

Females of many animal species mate with several different males, despite the extra costs. Recent studies in social insects now suggest that the resulting increase in genotypic variance in offspring is beneficial under selection by parasites. This finding also helps to understand the evolution and maintenance of sexual reproduction.

Animals↗

Sperm transfer and male competition in a bumblebee.

We investigated the dynamics of sperm transfer and the potential conflict between sexes over mating opportunities in the bumblebee, Bombus terrestris L. We recorded copulation duration in flight cages and manipulated copulation time by separating mating pairs. Sperm transfer and filling of the spermatheca were measured by dissecting queens at different time intervals after the onset of mating. On average, copulations lasted 37 min but most sperm were transferred into the female genital tract within the first 2 min. Sperm reached the spermatheca after 30-80 min. Males transferred a sticky gelatinous product of their accessory glands, the 'mating plug', to the female within 10-30 min of the onset of copulation. Hence the duration of the copulation matched the time required to deposit the plug fully. A likely function of the plug is to prevent backflow of sperm, but by artificially transferring mating plugs we showed that the plug also decreased sperm transfer into the female's spermatheca for at least 4 h and possibly for much longer (8 h or more). Increased mating costs arising from male selfishness may prevent females from seeking further matings. This may help to explain why females of B. terrestris seem to be mostly singly mated in the field, even though, in experiments with artificially inseminated queens, higher sperm diversity increases reproductive output. This is the first report of a mating plug for the Bombini but similar devices are known from two other tribes of the Apidae, the Apini and Meliponini. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

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 phi-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 haplo-types 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.

Journal Article↗