Communities within communes: Do bees’ social lives influence their gut bacteria?

ResearchBlogging.orgAs anyone who’s trying to sell you probiotic yogurt will tell you, what you can eat often depends on what’s living in your gut. For many animals, symbiotic bacterial communities help break down foods that would otherwise be indigestible. Perhaps most famously, termites would be unable to eat wood without specialized microbes in their guts [$a], but many other animals host bacteria that break down cellulose, the tough structural sugar of plant tissue, or to supply nutrients lacking in their diet.

This honeybee is carrying more than pollen. Photo by Danny Perez Photography.

The importance of gut microbes for digesting certain kinds of food has led to the suggestion that acquiring the right microbes can be an evolutionary key innovation—a change that creates access to new resources and spurs adaptive radiation. A 2009 study of gut microbes in ants found that evolutionary transitions to eating plants were associated with acquiring similar gut microbes.

So what about the biggest group of herbivorous hymenoptera, the bees? Bees’ ancestors were most likely predatory wasps, but some time in the Cretaceous Period they began making a living on pollen and nectar instead. A new study of gut microbes in a wide diversity of bees suggests that social organization, not diet, changed what lives inside bees’ bellies [$a].

The study examined the bacteria inside representatives of seven bee families, collecting sequence data from a gene widely used in studies of bacteria. The method employed allowed the authors to identify not just what kinds of bacteria were present, but how abundant each kind was. This microbial profile was specifically compared to the profile for Apis mellifera, the honeybee, whose gut microbes have been studied quite a bit already.

The bees form a monophyletic group—they all share a single common ancestor—and they are overwhelmingly herbivorous. Phylogenetic logic suggests, then, that any changes to the gut microbe community associated with the evolutionary transition to eating pollen and nectar would have occurred once, in the common ancestor. The microbes that facilitated that transition should also be widely shared by herbivorous bees.

In fact, most of the bee families sampled had little in common with the honeybees’ gut bacteria. Close relatives of the bacterial types found in Apis mellifera only turned up in two other Apis species, and bumble bees (genus Bombus). Since herbivory doesn’t explain this pattern of similarity (or lack thereof), the authors suggest that what really matters to bees’ guts is social behavior. Apis and Bombus are eusocial, forming hives of related workers cooperating to support a handful of reproductive individuals; the other bees surveyed in the study live mostly alone.

Life is different in the hive. Photo by stewickie.

As the authors note, eusociality would certainly change the environment offered to symbiotic bacteria. Bees in a hive should transmit bacteria among themselves, especially when feeding larvae. So eusocial bees mostly get their gut bacteria from their sisters. The bacteria in the guts of the solitary bees surveyed were mostly related to strains found in soil and on plants—so solitary bees are probably populating their guts with bacteria from their environment.

The idea that eusociality has shaped bees’ interactions with their symbiotic bacteria is interesting, but the data presented in this study are preliminary at best. The sampling of bee diversity presented here is broad, but not very deep—most of the bee families covered are represented by only one or two species. Understanding the effects of social structure on bees’ gut bacteria will take much finer-grained sampling to focus on evolutionary transitions not from predation to herbivory, but from solitary to eusocial lifestyles.

References

Kaltenpoth, M. (2011). Honeybees and bumblebees share similar bacterial symbionts. Molecular Ecology, 20 (3), 439-40 DOI: 10.1111/j.1365-294X.2010.04960.x

Martinson, V. G., B. N. Danforth, R. L. Minckley, O. Rueppell, S. Tingek, & N. A. Moran. (2011). A simple and distinctive microbiota associated with honey bees and bumble bees Molecular Ecology, 20 (3), 619-28 DOI: 10.1111/j.1365-294X.2010.04959.x

Ikeda-Ohtsubo, W., & A. Brune (2009). Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Molecular Ecology, 18 (2), 332-42 DOI: 10.1111/j.1365-294X.2008.04029.x

Russell, J., Moreau, C., Goldman-Huertas, B., Fujiwara, M., Lohman, D., & Pierce, N. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Nat. Acad. Sci. USA, 106 (50), 21236-41 DOI: 10.1073/pnas.0907926106

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Bees follow the crowd: Do whole-hive traits override individuals’ genetics?

ResearchBlogging.orgSocial insects are often considered prototypes of group selection, in which the evolutionary interests of individual organisms are forced to defer to the needs of their social group. Now, the authors of a new study of honeybees argue that colony-level traits can override the genetic predispositions of individual bees [$-a].


Do the needs of the many outweigh the needs of the one? Photo by Max_xx.

The study’s authors, Linksvayer et al.,
made use of artificially-selected colonies of bees that were first developed for a 1995 study [$-a]. The original selection experiment crossed queen bees with drones to create lines of honeybee colonies that collected and stored more pollen (“high pollen” lines) or less pollen (“low pollen” lines) than un-selected colonies do. The total amount of pollen a colony stores is supposed to be a “group” trait — an emergent property of the individual foraging decisions of every worker bee in the hive. But the genetics underlying that trait is encapsulated within the individual workers.

In the new experiment, Linksvayer et al. placed larvae from “high pollen” lines in “low pollen” colonies, and vice-versa. The larvae developed under the care of workers from the adoptive colony; when transplanted larvae reached adulthood, the team dissected them and measured the size of their ovaries — apparently big-ovaried workers collect lots of pollen. They found that “high pollen” larvae reared by “low pollen” workers had smaller ovaries than than those raised by workers of their own type. “Low pollen” larvae reared by “high pollen” workers didn’t end up with larger ovaries, though; and the “high pollen” larvae had substantially larger ovaries than the “low pollen” larvae regardless of who raised them.

There was a statistically significant effect of rearing environment, even if it was (apparently) entirely driven by the change seen in “high pollen” larvae. The authors conclude that this points to a mechanism whereby a bee colony keeps its workers in line with the colony-wide policy:

Thus, our results show that the network of social interactions that shapes development and expressed phenotypes has changed as a result of the colony-level selection program on pollen hoarding. Just as selection shapes physiological networks within organisms, our study shows that selection also shapes regulatory networks of superorganisms.

So the metaphor, then, is that the authors have observed in the hive something like what happens to a transplanted organ — the new host system incorporating the transplant for its own needs. I’m not sure the observed effect is strong enough to justify the meaning they assign to it; but it is an interesting observation.

As a postscript, I’m not sure social insects are a good model of group selection, because we know that they’re probably also experiencing kin selection, in which each worker’s fitness comes from helping the closely-related queen produce more sisters who share the same genes. Rarely, “anarchic” workers are born fertile and mate with drones [$-a] (there’s an open-access paper on the genetics underlying this trait); but in hives without anarchists, “group fitness” is hard to separate from the fitness of individual workers. A paper published in Nature this June showed that in another classic group selection system (parasites within a single host) kin selection is really the more important process.

References

Linksvayer, T., Fondrk, M., & Page Jr., R. (2009). Honeybee social regulatory networks are shaped by colony-level selection. Am. Nat., 173 (3) DOI: 10.1086/596527

Oldroyd, B., Smolenski, A., Cornuet, J., & Crozler, R. (1994). Anarchy in the beehive. Nature, 371 (6500) DOI: 10.1038/371749a0

Oxley, P., Thompson, G., & Oldroyd, B. (2008). Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera). Genetics, 179 (3), 1337-1343 DOI: 10.1534/genetics.108.087270

Page, R., & Fondrk, M. (1995). The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding Behavioral Ecol. & Sociobiol., 36 (2), 135-44 DOI: 10.1007/BF00170718

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