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Genetic and genomic analyses of the division of labour in insect societies

Key Points

  • With a rich and well understood natural history and a long tradition of being used to address fundamental issues in development, neuroscience, behaviour, ecology and evolution, social insects are now emerging as important model systems for genetic and genomic analyses of complex traits, namely, the remarkably diverse and intricate systems of division of labour exhibited by the ants, bees, wasps and termites.

  • Hereditary effects on division of labour are more pervasive than previously supposed. The genes that underlie hereditary effects on division of labour have yet to be identified.

  • Hereditary effects on division of labour raise the spectre of conflict between those that are reproducing and those that are not, but it seems that mechanisms have evolved in many species to minimize conflict while still preserving genetic diversity and its potential benefits to colony life.

  • Hereditary effects on one form of division of labour, that is, queen–worker caste determination, have another cost: decreased caste-ratio flexibility. Some findings suggest that environmental factors mitigate this genetic bias, but more research is needed.

  • Hereditary effects on another form of division of labour, that is, worker–worker specialization, benefit colonies by increased efficiency of division of labour or increased colony homeostasis.

  • Molecular analyses of candidate genes and gene expression profiling reveal that the same set of highly conserved molecular pathways (for example, insulin) are involved in the regulation of different forms of division of labour, even across distantly related social insect taxa that evolved eusociality independently.

  • Some of these pathways are related to the fundamental processes of nutrition, metabolism and reproduction, supporting the idea that life-history traits of solitary insects that are related to these processes could have served as evolutionary precursors to eusociality.

  • The sequencing of the first social insect genome, that of the honeybee, has led to several important findings, including the discovery that the molecular basis of queen–worker caste determination involves insulin signalling and epigenetic regulation.

  • We predict that there will be whole genome sequences for 10–20 social insect species and their relatives within the next 10 years, and these could be strategically chosen to span the full range of sociality — from solitary to eusocial — to provide powerful resources to study the mechanisms and evolution of division of labour.

Abstract

Division of labour — individuals specializing in different activities — features prominently in the spectacular success of the social insects. Until recently, genetic and genomic analyses of division of labour were limited to just a few species. However, research on an ever-increasing number of species has provided new insight, from which we highlight two results. First, heritable influences on division of labour are more pervasive than previously imagined. Second, different forms of division of labour, in lineages in which eusociality has arisen independently, have evolved through changes in the regulation of highly conserved molecular pathways associated with several basic life-history traits, including nutrition, metabolism and reproduction.

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Figure 1: Caste and division of labour in insect societies.
Figure 2: Fruits of sociality.

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Acknowledgements

We thank the students participating in the reading group of the Illinois Social Insect Training Initiative for helpful and stimulating discussion during the conception of this Review, and S. A. Cameron, C. M. Grozinger, members of the Suarez and Robinson laboratories, and three anonymous reviewers for comments that improved the manuscript. Research by the authors was supported by grants from the National Institutes of Health, the National Science Foundation, the United States Department of Agriculture and Burroughs Wellcome Trust (G.E.R.), the Illinois Sociogenomics Initiative (G.E.R.), the National Science Foundation (A.V.S.) and the University of Illinois Graduate College (C.R.S.).

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Glossary

Division of labour

A social system in which individuals specialize in specific occupations. In insect societies, queens mostly reproduce, whereas workers engage in all tasks related to colony growth and development. Young workers tend to work in the nest, whereas older individuals forage outside the nest.

Queen

Individual(s) that produces most or all of the offspring in a social insect colony.

Worker

Individual that performs all tasks related to the growth and development of a social insect colony; engage in little, if any, personal reproduction.

Caste

Term used to describe a group of individuals in social insect colonies that specializes to some extent in specific occupations as a result of division of labour. Social insect castes can be associated with differences in age, anatomy and morphology.

Eusocial

Traditionally defined as social species that show three features: extreme asymmetries in reproduction, with some individuals reproducing a great deal and others little or not at all; overlapping generations of adults in the nest; and cooperative care of offspring.

Age polyethism

Change in behaviour with age; a term used primarily to describe behavioural maturation in some species of social insect workers.Results in age-related division of labour at the colony level.

Superorganism

A metaphor for a colony of social insects that highlights three key characteristics: first, the colony functions as a single, highly integrated unit; second, natural selection acts on the colony; and third, a relative lack of competition among individuals.

Polyandry

Multiple mating by females.

Social hybridogenesis

Only hybrid matings can produce workers; non-hybrid matings produce queens. It is similar to hybridogenesis in solitary species, whereby hybrid matings produce viable hybrid offspring, but the germ line is purely parental.

Thelytokous parthenogenesis

Production of females from unfertilized eggs (asexual reproduction).

Haplodiploid

A genetic system in which females develop from fertilized, diploid eggs and males develop from unfertilized, haploid eggs. In Hymenoptera (ants, bees and wasps), sex determination can occur through a single locus (although multiple loci exist in some species); heterozygotes are female and hemizygotes are male.

Kin selection

W. D. Hamilton's theory to explain the evolution of the hallmark of social life: altruistic cooperation (performing acts that are costly to the benefactor but that benefit others). For example, by helping a relative, an individual increases its fitness by increasing the number of copies of its genes in the population.

Colony-level selection

A special form of group (family) selection, first described by Charles Darwin, to explain the evolution of sterile workers in insect societies.

Diapause

Dormancy owing to unfavourable environmental conditions.

Storage proteins

Circulating lipoproteins used by insects to store nutrients.

Gynes

In insect societies, females that are destined to become queens.

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Smith, C., Toth, A., Suarez, A. et al. Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9, 735–748 (2008). https://doi.org/10.1038/nrg2429

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