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Associations with symbiotic microorganisms are a major source for evolutionary innovation in eukaryotes. Arthropods have long served as model systems to study such associations, especially since Paul Buchner’s (1965) seminal work that beautifully illustrated the enormous diversity of microorganisms associated with insects. Particularly high taxonomic and functional diversities of microbial symbionts have been found in the guts and gut-associated organs of insects. These microorganisms play important roles in the digestion, nutrition and defence of the host. However, most studies of gut microorganisms have focused on single host taxa, limiting the ability to draw general conclusions on composition and functional roles of the insect gut microbiota. This is especially true for the diverse and important insect order Hymenoptera that comprises the bees, wasps and ants. Recently, Russell et al. (2009) analysed the bacterial community associated with diverse ant species and found evidence for changes in the microbial gut community coinciding with the evolution of herbivory. In this issue of Molecular Ecology, Martinson et al. (2011) provide the first broad-scale bacterial survey for bees. Their findings substantiate earlier evidence for a surprisingly simple gut microbiota in honeybees (Apis mellifera) that is composed of only six to ten major phylotypes. Importantly, Martinson et al. demonstrate for the first time that the same bacterial phylotypes are major constituents of other Apis as well as Bombus species, but not of any other bees and wasps outside of the corbiculate bees, a clade of four tribes within the subfamily Apinae. These results indicate that corbiculate bees harbour a specific and possibly co-evolved bacterial community in their digestive tract. Furthermore, the comparison with other bees and wasps suggests that changes in social lifestyle may have had a stronger effect on the evolution of the gut microbiota than the dietary shift from predatory ancestors to pollen-feeding (i.e. herbivorous) species. These findings have far-reaching implications for research on the microbial symbionts of insects as well as on the nutritional physiology of the ecologically and economically important group of corbiculate bees.
Bees are the most important plant pollinators on earth, as they are essential for the sexual reproduction of much of the natural vegetation surrounding us as well as many agricultural crops (Michener 2000) (Fig. 1). They show a diversity of social lifestyles, ranging from solitary individuals to highly eusocial colonies with a single queen and up to 100 000 nonreproductive workers (Michener 2000). Nearly all extant bees are herbivores that exploit pollen as their sole protein source. They evolved from predatory digger wasp-like ancestors in the early Cretaceous, about 100 million years ago (Poinar & Danforth 2006). The dramatic shift to a completely herbivorous diet likely required major adaptations in the nutritional physiology of the early bees. Similar dietary transitions from predation to herbivory in ants and from phloem- to xylem-feeding in sharpshooters have been accompanied by a change in the symbiotic microbiota of the host insects (Moran 2007; Russell et al. 2009). Martinson et al. (2011) for the first time investigated the microbial community associated with a large number of bee species to test the hypothesis that bacterial symbionts have played a key role in the shift from predatory ancestors to a herbivorous lifestyle in this important group of insects.
Figure 1. Bumblebees (Bombus spp.) and honeybees (Apis spp.) are associated with comparatively simple communities of microorganisms. Interestingly, they share several bacterial symbionts that seem to be specific for this group of corbiculate bees and do not occur in any other species of bees (pictures kindly provided by Sabine Radmacher).
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For the analysis of the microbial community of bees, Martinson et al. (2011) collected specimens of 55 bee and four wasp species. Using PCR with general eubacterial primers and subsequent cloning and sequencing, they generated almost 5000 near-full length bacterial 16S rRNA sequences from 17 of the bee and three of the wasp species and complemented this data set with over 600 already published sequences that originated mostly from Apis mellifera-associated bacteria. Almost all of the sequences the authors obtained for A. mellifera corresponded to eight bacterial phylotypes that had been described previously, supporting the view that honeybees harbour a distinctive and relatively simple bacterial community. Interestingly, some of these phylotypes were also present in closely related corbiculate bees of the genera Apis and Bombus, although none of these species carried the same microbial community as A. mellifera. However, a comparison of the bacterial communities across all of the bee species revealed no common subset of bacterial taxa, prompting the authors to reject the hypothesis that the evolution of a specific microbiota was required for the shift to pollen-feeding.
To screen a larger sample of bee and wasp species for the presence of the A. mellifera phylotypes, the authors designed diagnostic primers based on the 16S rRNA sequences. Surprisingly, each of the six corbiculate bee species (three Apis spp. and three Bombus spp.) harboured at least one of the honeybee phylotypes, respectively, while these were never detected in any other species of bees and wasps tested. This result is highly interesting, because it suggests a specific and possibly co-evolved association between corbiculate bees and their gut microbiota. Although symbioses between insects and extracellular gut bacteria have traditionally been regarded as evolutionarily labile, recent studies provide accumulating evidence for the long-term stability of several such interactions in different insect orders (Hosokawa et al. 2006; Kikuchi et al. 2009; Russell et al. 2009). In this context, the study by Martinson and colleagues constitutes an important contribution by providing one of the first community-wide analyses suggesting co-evolution between hosts and their microbiota.
In the light of the consistent association of specific phylotypes with the honeybee and other corbiculate bees, Martinson et al. speculate on the function of the gut microbiota in bees. As in many other insects, the symbionts could be involved in the nutritional upgrading of the restricted diet or in the digestion of otherwise inaccessible diet, in the case of the bees the persistent pollen grains. Even more interestingly, however, the symbiotic community could play a vital role for the defence of the individual bee or the entire colony. On the individual level, gut bacteria can provide an important line of defence against invading pathogens, which has been shown for both invertebrate and vertebrate hosts (e.g. Tancrede 1992; Dillon & Dillon 2004). Living in large colonies, social bees additionally face the problem of pathogen spread among nestmates as well as the risk of microbial infestation of their larval provisions. Several other insect taxa with mass storage of larval provisions are known to cultivate microbial symbionts that defend the food resources or the host offspring against pathogen attack (Kaltenpoth 2009). Elucidating the functional roles of microorganisms associated with honeybees and their possible significance for colony health will be especially important in the light of declining bee populations due to pathogen pressures or anthropogenic influence. The work by Martinson et al. lays the foundation for such functional analyses.
This study has important implications for the field of insect symbiosis research. Although much is known about the nature and function of individual symbionts in insect hosts, comparative analyses of complete microbial communities remain scarce. Broad-scale comparisons across insect taxa like the one provided by Martinson et al. are urgently needed to characterize the diverse microbiota associated with insects and to provide the basis for investigating the complex interactions among symbionts and the consequences of these interactions for the host. The increasing affordability of large-scale sequencing projects will certainly pave the way for further comparative studies of multipartite insect–bacteria symbioses.