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Eusocial insects as emerging models for behavioural epigenetics

This article has been updated

Key Points

  • The combination of accessible next-generation sequencing technologies and advanced genetic tools holds promise to increase the tractability of eusocial insects for research into the genetic and epigenetic regulation of social behaviour.

  • Epigenetic processes — including transcription factor binding, histone post-translational modifications, DNA methylation and regulation by non-coding RNAs — function in concert to stabilize phenotypic responses to transient environmental cues by inducing and maintaining associated gene expression patterns.

  • Genetic and environmental factors have complementary roles in shaping morphology and behaviour in eusocial insects. Epigenetic response thresholds determine an individual's sensitivity to environmental cues and the age at which behavioural transitions occur.

  • Pharmaceutical compounds and RNA interference (RNAi) are currently used to change gene expression in somatic cells to alter caste fate and behaviour in eusocial insects. In addition, the intrinsic features of a select group of eusocial species — including representatives from the bee, ant, wasp and termite lineages — allow the possibility for researchers to carry out sophisticated genetic manipulations.

Abstract

Understanding the molecular basis of how behavioural states are established, maintained and altered by environmental cues is an area of considerable and growing interest. Epigenetic processes, including methylation of DNA and post-translational modification of histones, dynamically modulate activity-dependent gene expression in neurons and can therefore have important regulatory roles in shaping behavioural responses to environmental cues. Several eusocial insect species — with their unique displays of behavioural plasticity due to age, morphology and social context — have emerged as models to investigate the genetic and epigenetic underpinnings of animal social behaviour. This Review summarizes recent studies in the epigenetics of social behaviour and offers perspectives on emerging trends and prospects for establishing genetic tools in eusocial insects.

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Figure 1: Epigenetic response threshold model of behavioural plasticity.
Figure 2: Epigenetic mechanisms of gene regulation in the insect brain.
Figure 3: Genetic approaches in eusocial insects.

Change history

  • 11 September 2014

    The postal addresses for some of the authors' affiliations have now been corrected to "Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, New York 10016, USA"; "Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA"; and "Epigenetics Program, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA".

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Acknowledgements

The authors thank the three anonymous reviewers and R. Graham for their insightful critiques and suggestions in improving an earlier version of this manuscript. This work has been supported by a Howard Hughes Medical Institute Collaborative Innovation Award (HCIA) #2009005 to D.R., S.L.B. and J.L.

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Glossary

Social behaviours

The interactions among individuals of the same species, for example, collaboration within a well-defined group such as a colony of eusocial insects.

Polyethism

Variation in the allocation of nest-related tasks among individuals in a colony. Polyethism typically refers to the special case of age-dependent changes in an individual's behaviour (that is, age-dependent or temporal polyethism); however, it more generally denotes differences in behaviour associated with caste (that is, temporal as well as morphological or physical polyethism).

Castes

Specialized behavioural groups within a eusocial colony that often correspond to morphological features and that are generally considered to be a stable, if not permanent, characteristic of an individual. For example, members of the queen caste hatch as adults with wings and can reproduce, whereas members of the worker caste (or castes) are wingless and do not normally reproduce.

Behavioural epigenetics

An emerging multidisciplinary field of research that aims to understand how epigenetic processes transform transient environmental cues into persistent molecular patterns of gene expression in order to modulate animal behaviour.

Queen

A morphologically and/or behaviourally distinct reproductive caste in eusocial insects that often shows specialization in both reproduction and dispersal abilities. Depending on the species, a colony may contain one queen (monogyny) or multiple queens (polygyny). Queens, together with males, constitute the 'germline' of a eusocial insect colony.

Worker

A non-reproductive caste in eusocial insects. Workers cooperatively care for the brood of the colony, forage for food, clean up the nest and defend it against invaders. Workers constitute the body or 'soma' of a eusocial insect colony.

Royal jelly

A nutrient-rich secretion produced by mandibular and hypopharyngeal glands in honeybee nurses, which feed it to larvae to induce their development into gynes (that is, virgin queens).

Gamergates

A unique reproductive caste comprised of mated, fertile workers. In some ponerine species (for example, Harpegnathos saltator), gamergates emerge from the existing cohort of workers when a queen dies or is artificially removed from a colony.

Parthenogenetic

Pertaining to parthenogenesis, which is a form of asexual reproduction that produces viable embryos from eggs without fertilization by sperm — notably, haploid male production in Hymenoptera. In some parthenogenetic insects such as Cerapachys biroi, female reproductives can lay diploid eggs by thelytoky, thereby producing clonal female offspring.

Thelytokous

The parthenogenetic production of female offspring from unfertilized eggs.

Major worker

(Also known as a soldier). A large worker produced in some ant species, for example, Camponotus floridanus and Pheidole morrisi. Major workers are typically aggressive and specialize in nest defence and carrying heavy or large food items.

Minor worker

A small worker produced in some ant species, for example, Camponotus floridanus and Pheidole morrisi. Minor workers carry out most tasks in the nest, including foraging.

DNA methyltransferase

An enzyme that catalyses DNA methylation. There are two functional DNA methyltransferase (DNMT) classes in metazoa. DNMT1 carries out maintenance DNA methylation using a pre-methylated DNA sequence as a template, whereas DNMT3 is responsible for de novo methylation of DNA. DNMT2 was originally defined as a DNA methyltransferase but was later correctly recognized as a tRNA methyltransferase.

CpG island

An intergenic genomic region that contains a greater density of unmethylated CG dinucleotides than expected compared with genome-wide density. CpG islands were originally defined as regulatory regions in mammals. As insects largely lack intergenic DNA methylation, it remains unclear whether CpG island-like sequences are functional in insects.

Allozyme

A variant form of an enzyme that is encoded by a different allele of the same genetic locus. Allozyme analysis was used to infer genetic variation before direct DNA sequencing became widely used.

Kin selection

A form of natural selection that favours the reproductive success of relatives even at a cost to an individual's own survival and reproduction.

Inclusive fitness

The sum of the reproductive fitness of an individual and the indirect fitness received by relatives other than the individual's own offspring that were produced as a result of help from the individual.

Haplodiploid

A genetic system of sex determination that is mainly found in the insect order Hymenoptera, including ants, bees and wasps. Hymenopteran females are diploid (that is, they have two complete sets of chromosomes), whereas males are normally haploid and have only one set of chromosomes. Some species, such as the fire ant Solenopsis invicta, also produce viable diploid males.

Relatedness asymmetries

Differences in the degree of genetic similarity between parents and offspring that arise in eusocial insects owing to the haplodiploid mode of sex determination and that is exacerbated by polyandry (a form of polygamy in which a female mates with multiple males).

CRISPR–Cas

(Clustered regularly interspaced short palindromic repeat–CRISPR-associated). A technique for generating site-specific mutant or transgenic organisms using the Cas9 protein–guide RNA complex to generate mutations or to direct exogenous DNA to specific genomic regions where it is incorporated.

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Yan, H., Simola, D., Bonasio, R. et al. Eusocial insects as emerging models for behavioural epigenetics. Nat Rev Genet 15, 677–688 (2014). https://doi.org/10.1038/nrg3787

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