Eusocial Insect Evolution

Also see:
Tree of Life - Subphylum Hexapoda

Prevalence of Insect Eusociality

Eusociality generally affords a great survival advantage to any group of animals, and is likely best exemplified in insects. Behavioral characteristics include the cooperative care of offspring, distinct castes of workers (often sterile) that do not sexually reproduce and groups that do, and well defined divisions of labor. The behaviors of distinct groups are genetically coded, and one caste has lost the ability to perform functions of other castes. Eusociality is highly refined and abundant in insect Order Hymenoptera (the ants, bees and wasps), as well as in Infraorder Isoptera, Order Blattodea (the termites). There are also eusocial, aphids, and thrips. However, there is considerable differentiation between species in extent and type of eusocial behavior. Among the hymenopterans, ants are far and away the most social (almost all species), most having highly refined labor division, and have even been noted for collective colonial problem solving. Bees and wasps as a group are far less social, with some highly social lineages, and other lineages having entirely solitary behavior. The Isopterans are highly eusocial, where a single king and queen perform all reproduction, and there are castes of workers and soldiers.

Darwin's Problem and the Genetic Basis of Eusocial Traits

The high prevalence of eusociality among hymenopterans compared to its general rarity within the animal kingdom has been an area of debate in evolutionary biology, and the new genomics sequencing technologies are enabling its study in detail. In a simple view of Darwinian evolution, such altruistic self-sacrificing of one’s own genes could be viewed as contradictory. But, according to Hughes (et al., 2008), eusociality evolved eight to ten times within Hymenoptera. In The Origin of Species, Darwin described sterile worker castes in the social insects as "the one special difficulty, which at first appeared to me insuperable and actually fatal to my whole theory". The dilemma has been explained by the concept of “inclusive fitness” a combination of individual reproductive success and reproductive success of a group having similar genes. In simple mathematical terms, the portion of the altruist’s genes that are passed on exceeds those that would be passed on in an individual effort to procreate. We now know it’s more complex than this due to females having diploid cells (having two homologous copies of each chromosome, one from each parent), and males having haploid cells (with but one chromosome). Consequently, males share only 25% of their sisters' genes, whereas females on average share 50% of their sister's genes, which is the same as it would be with their own offspring. Evolution will select for altruistic cooperation when it's more efficient to raise siblings than offspring, providing a sustainable selective advantage of eusociality because the collective expends less energy per offspring by its cooperative behaviors and division of labor. The relatedness of sisters diminishes should the queen not be sexually monogamous. Interestingly, many ants, bees, and wasps have evolved behavior of lifetime monogamy, where the queen mates with one and only one male, who dies afterwards. This monogamous trait is an ancestral characteristic in all eusocial Hymenopteran lineages (Hughes, 2008).

Basic Natural Selection in Evolution of Eusocial Altruism

The above explains the genetic basis for eusocial behavior being maintained in a lineage, but how did it arise? That would be fairly straightforward natural selection. First, some advantage was accrued by common nesting, and selected for. Mutations and selection led to selective silencing of genes for individual wandering (e.g., loss in wings in worker castes). Behavior beneficial to the queen’s reproduction is reinforced. Finally, colonial lineages that are eusocial outcompete those that are not.

Recent Evolutionary Biology Studies of Eusocial Behavior, Enter Sociogenomics

Recent research has been powered by modern high-throughput molecular technology that can quickly and inexpensively measure the expression of all genes, or all protein, or entire genome sequences, leading to dramatics new insights. Epigenomics that studies the interaction of genes and environment has been particularly important, as well as roles played by DNA methylation, and microRNA-guided, novel post-transcriptional modifications (i.e., same gene, but different resulting proteins). A range of finding have emerged in the last decade, such as: 1) Each eusocial insect lineage evolved from a solitary common ancestor a species in which a single genome produced a single adult phenotype; 2) Transcriptomes studies support wasps as the oldest eusocial group, with bees and ants having branched from the wasp lineage around 145 million years ago at the very lowest Cretaceous Period; 3) Sociality started simple, but became increasing complex as genomes were further shaped and thus eusociality refined by natural selection, where today some 14,000 eusocial hymenopteran species span a wide spectrum of eusocial behavioral traits; 4) some genes important in the eusocial phenotype lack homology across species, indicating recent rapid evolution. As of 2014, entire genomes were available for 11 eusocial hymenopteran orders. Gene expession measurements enable statistical determination of which genes are likely involved in modulating eusocial behavior, and which genes have been modified through selection for different behavior.

Social Insect Fossils
Flying termite (or Alate) in amber.	Wasp Lower Cretaceous Liaoning Province, China	Wasp Lower Cretaceous Crato Formation, Brazil	Soldier termites in Colombian amber

References:

• Hughes, W. O. H.; Oldroyd, B. P.; Beekman, M.; Ratnieks, F. L. W. (2008). "Ancestral Monogamy Shows Kin Selection is Key to the Evolution of Eusociality". Science 320 (5880): 1213–1216.
• G.E. Robinson et al., “Sociogenomics: social life in molecular terms,” Nat Rev Genet, 6:257-70, 2005.
• P.G. Ferreira et al., “Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes.” Genome Biol, 14:R20, 2013.
• B.R. Johnson et al., “Phylogenomics resolves evolutionary relationships among ants, bees, and wasps,” Curr Biol, 23:2058-62, 2013.
• S.H. Woodard et al., “Genes involved in convergent evolution of eusociality in bees,” PNAS, 108:7472-77 2011.
• B.R. Johnson, N.D. Tsutsui, “Taxonomically restricted genes are associated with the evolution of sociality in the honey bee,” BMC Genomics, 12:164, 2011.
• B. Feldmeyer et al., “Gene expression patterns associated with caste and reproductive status in ants: worker-specific genes are more derived than queen-specific ones,” Mol Ecol, 23:151-61, 2014.
• S. Patalano et al., “Shifting behaviour: epigenetic reprogramming in eusocial insects,” Curr Opin Cell Biol, 24:367-73, 2012.
• H. Yan et al., “Eusocial insects as emerging models for behavioural epigenetics,” Nat Rev Genet, 15:677-88, 2014.
• R. Kucharski et al., “Nutritional control of reproductive status in honeybees via DNA methylation,” Science, 319:1827-30, 2008.
• B.R. Herb et al., “Reversible switching between epigenetic states in honeybee behavioral subcastes,” Nat Neurosci, 15:1371-73, 2012.
• H.E. Amarasinghe et al., “Methylation and worker reproduction in the bumble-bee (Bombus terrestris),” Proc Roy Soc B, 281:20132502, 2014.
• A. Spannhoff et al., “Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees,” EMBO Rep, 12:238-43, 2011.
• D.F. Simola et al., “Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality,” Genome Res, 23:1235-47, 2013.
• J.K. Greenberg et al., “Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome,” Genes Brain Behav, 11:660-70, 2012.
• L.G. Hernández et al., “Worker honeybee brain proteome,” J Proteome Res, 11:1485-93, 2012.