Ants, Bees, Genomes & Evolution @ Queen Mary University London


Published: 23 January 2007

Behavioral Genomics: A, Bee, C, G, T

Yannick Wurm, John Wang, Laurent Keller

Current Biology, 2007, 17:R51-3


Honeybees, termites and ants occupy the ‘pinnacle of social evolution’ with societies of a complexity that rivals our own. The sequencing of the honeybee genome will provide a strong foundation for studying the genetic basis of complex social behavior.

Go to the ant, thou sluggard; consider her ways, and be wise

Proverbs 6:6

This well-known Bible verse appropriately illustrates the long fascination of human beings for the complexity of social insect colonies and the industrious nature of their workers. The major organizing principle of ant, bee and termite societies is reproductive division of labor whereby one or a few individuals, the queens, specialize in reproduction while the others, the workers, participate in cooperative tasks such as building the nest, collecting food, rearing the young and defending the colony. This social organization provides numerous advantages and is the basis for the tremendous ecological success of social insects [1]. The sequencing of the honeybee genome [2] is an exciting step towards uncovering the molecular events underlying the evolution of altruism and complex behaviors.

A genome sequence, like a honeybee queen, is useless if it is not accompanied by the assiduous labor of a large number of cooperative workers. For this reason, an industrious swarm of scientists has collaborated to conduct detailed analyses and comparisons of the honeybee genome with those of model organisms, in particular the fruitfly Drosophila melanogaster. These analyses, reported in no fewer than 40 companion papers published in Science, PNAS and special issues of Genome Research and Insect Molecular Biology, have revealed many interesting features associated with the unusual social biology of the honeybee.

To date, most of our understanding of behavioral genetics has come from studies in model organisms such as D. melanogaster and C. elegans. In only a handful of cases, however, have genetic variants been shown to be responsible for behavioral differences observed under natural conditions [3, 4]. An interesting feature of the honeybee is that workers change tasks as they age. They typically remain in the nest when young and then switch to dangerous tasks outside the nest only when they are older. This switch can be manipulated by altering colony needs or by treatment with chemicals that cause precocious foraging. Capitalizing on this, Whitfield et al. [5] conducted a series of clever experiments to separate the effects of worker age, genotype, environment and experience on gene expression. They found that the transition from hive work to foraging is accompanied by a robust molecular signature with many genes sharing the same expression pattern across the conducted experiments. Examination of these genes revealed shared cis-regulatory promoter elements that may be responsible for their co-regulation [6]. This is a big step towards clarifying the regulatory cascades governing the networks of behavioral genes. Future investigations into the neuronal circuitry of bees and its modulation should also be facilitated by the bioinformatic and proteomic identification of 36 prohormones coding for more than 200 neuropeptides [7].

Comparison of the honeybee genome to that of other insects revealed a number of interesting differences. Not a complete surprise was the identification of nine new genes linked to the production of royal jelly, which workers feed to the queen and larvae. These genes apparently evolved from a single progenitor gene which encodes a member of the ancient Yellow protein family [8]. Similarly, the striking expansion of the odorant receptor family in honeybees (170 genes) relative to D. melanogaster (62) and the mosquito Anopheles gambiae (79) [9] makes sense given the prime role of pheromones in communication and the need for workers to discriminate between diverse floral odors. These discoveries should help elucidate some of the bees’ fascinating skills, which include precise memory of space and odors as well as the abstract modeling and linguistic abilities shown by the ‘waggle-dance’.

A more surprising finding was that honeybees have only half as many immune defense genes as D. melanogaster or A. gambiae. Many authors have suggested that colonies of social insects should be under particularly strong pathogenic pressure because numerous highly related individuals live in close quarters. Although not frequently recognized, however, bees spend most of their lives in a protected colony environment, while flies and mosquitoes grow up in rotting food or stagnant water. Moreover, the food provided to bee larvae has already been processed by adults and thus is less likely to contain pathogens. Likewise, the risk of poisoning or infection may be low when foraging nectar and pollen from flowers with which a mutualism has evolved [10]. The close association between bees and plants, and the lack of incentive for plants to produce toxic nectar or pollen may actually also explain the a priori surprising finding that honeybees have far fewer gustatory receptors than D. melanogaster and A. gambiae [9]. Another possible explanation for why bees have fewer immune defense genes is that they display social behaviors such as extensive grooming and ‘social fever’ that may effectively combat infections [10].

The honeybee genome has provided several interesting revelations concerning the most unusual characteristic of social insects: their ability to produce very different phenotypes from the same genotype as a result of the alternative developmental programs followed by queens and workers. Indeed, in several ant species, queens can differ dramatically in size and morphology from workers, yet almost nothing is known about the epigenetic factors underlying the developmental switch responsible for these differences. Of particular interest was the discovery of 65 microRNAs, including some that show caste-specific expression patterns during development [2]. This raises the exciting possibility that microRNAs are involved in caste determination via differential gene expression between queens and workers.

The finding that the honeybee genome harbors genes encoding a complete set of methyltransferases, the highest known eukaryotic CpG content, and evidence for CpG methylation of protein coding genes is also of great interest, given that methylation of CpGs represses transcription in mammals. Interestingly, in contrast to mammals, in the honeybees DNA methylation was detected predominantly in coding regions. Perhaps methylation plays a role in regulating genes involved in developmental differences between honeybee queens and workers [11]. Finally, it appears that more than 60 genes are duplicated specifically in the honeybee, including two genes for components of the insulin pathway [2]. This pathway regulates growth in other animals [12] and could be the means through which queen bees become bigger than workers [13]. These and/or other duplicated genes may be involved in caste or sex determination and differences, and/or in social interactions.

Comparative analyses revealed some other peculiar genomic features including the fact that the honeybee genome evolves at a much slower rate than the strongly derived genomes of flies and mosquitoes. This is evidenced by sequence identity, intron conservation, and gene loss relative to an ancestor common to insects and vertebrates [2]. The slow evolution of the honeybee genome may be general to hymenopteran insects, whose haplo-diploid sex-determination system might purge deleterious mutations that would be masked in diploid individuals [2]. Alternatively, it could be due to the long generation time of social insects — queens typically can live many years [14] — and/or to the low effective population size resulting from a single individual monopolizing reproduction in the hive.

Interestingly, these characteristics may also be responsible for another idiosyncrasy of the honeybee, the very high average recombination rate of 5.7 recombinations per chromosome [15]. Such a high recombination rates has only been reported in one other species, the ant Acromyrmex echinator [16]. High recombination rates might thus be a characteristic of social insects, again perhaps a result of their typically long generation time and small population size. Alternatively, high recombination rates might have been selected as a means to increase genetic diversity among offspring.

Another striking finding was that the honeybee genes controlling circadian rhythm and telomere length are more similar to vertebrates than to D. melanogaster or A. gambiae [2]. Drosophila is considered the paradigm of insect biology. This clearly needs to be changed given the increasing evidence that many of Drosophila’s features, such as their early-acting axis specification genes, are highly derived and not characteristic of insects.

The honeybee genome sequence and attendant analyses and experiments open many avenues for future research. In anticipation of a finished genome, the BeeSpace project has begun the dissection of environmental and hereditary influences on brain gene expression in the context of defensive behavior and foraging using thousands of microarrays (G. Robinson, personal communication). Beyond division of labor and cooperation within a colony, it will be exciting to understand the molecular basis of the evolution of within-colony conflicts and their resolution. Functional tests, through ectopic expression or repression of genes involved in both behavior and caste development, will be essential in elucidating how insect societies function.

At a more basic level, the mechanisms by which solitary species became social could be pinpointed by examining either facultatively social species or contrasting pairs of solitary and primitively social species. The independent evolution of social life in bees, ants, wasps and termites also provides a unique opportunity to determine whether the convergent morphological, physiological and behavioral adaptations that have occurred in these taxa are due to modification of the same developmental pathways and gene networks. The recent development of an EST library, microarray and other molecular genetic tools for the fire ant, Solenopsis invicta (our group’s unpublished data), should pave the way for such sociogenomic comparative studies.


References

  1. Hölldobler B. Wilson E.O. The Ants. Belknap Press, 1990

  2. The Honeybee Genome Sequencing Consortium Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006; 443: 931-949

  3. Osborne K.A. Robichon A. Burgess E. Butland S. Shaw R.A. Coulthard A. Pereira H.S. Greenspan R.J. Sokolowski M.B. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science. 1997; 277: 834-836

  4. Keller L. Ross K.G. Selfish genes: a green beard in the red fire ant. Nature. 1998; 394: 573-575

  5. mWhitfield C.W. Ben-Shahar Y. Brillet C. Leoncini I. Crauser D. LeConte Y. Rodriguez-Zas S. Robinson G.E. Genomic dissection of behavioral maturation in the honey bee. Proc. Natl. Acad. Sci. 2006; 103: 16068-16075

  6. Sinha S. Ling X. Whitfield C.W. Zhai C. Robinson G.E. Genome scan for cis-regulatory DNA motifs associated with social behavior in honey bees. Proc. Natl. Acad. Sci. 2006; 103: 16352-16357

  7. Hummon A.B. Richmond T.A. Verleyen P. Baggerman G. Huybrechts J. Ewing M.A. Vierstraete E. Rodriguez-Zas S.L. Schoofs L. Robinson G.E. et al. From the genome to the proteome: uncovering peptides in the Apis brain. Science. 2006; 314: 647-649

  8. Drapeau M.D. Albert S. Kucharski R. Prusko C. Maleszka R. Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honey bees. Genome Res. 2006; 16: 1385-1394

  9. Robertson H.M. Wanner K.W. The chemoreceptor superfamily in the honey bee Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Res. 2006; 16: 1395-1403

  10. Evans J.D. Aronstein K. Chen Y.P. Hetru C. Imler J.L. Jiang H. Kanost M. Thompson G.J. Zou Z. Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect. Mol. Biol. 2006; 15: 645-656

  11. Wang Y. Jorda M. Jones P.L. Maleszka R. Ling X. Robertson H.M. Mizzen C.A. Peinado M.A. Robinson G.E. Functional CpG methylation system in a social insect. Science. 2006; 314: 645-647

  12. Wu Q. Brown M.R. Signaling and function of insulin-like peptides in insects. Ann. Rev. Entomol. 2006; 51: 1-24

  13. Wheeler D.E. Buck N. Evans J.D. Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect. Mol. Biol. 2006; 15: 597-602

  14. Keller L. Genoud M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature. 1997; 389: 958-960

  15. Beye M. Gattermeier I. Hasselmann M. Gempe T. Schioett M. Baines J.F. Schlipalius D. Mougel F. Emore C. Rueppell O. et al. Exceptionally high levels of recombination across the honeybee genome. Genome Res. 2006; 16: 1339-1344

  16. Sirvio A. Gadau J. Rueppel O. Lamatsch D. Boomsma J.J. Pamilo P. Page Jr., R.E. High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J. Evol. Biol. 2006; 19: 1475-1485


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DOI: https://doi.org/10.1016/j.cub.2006.12.019

© 2007 Elsevier Ltd. Published by Elsevier Inc.

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