Harpegnathos saltator, more commonly known as Indian jumping ants, display a unique ability to change social functional group (caste) during their lifetime.
This phenomenon is observed following the death or removal of the queen from the colony, in which a brief but intense period of duelling tournaments between workers results in the emergence of a several dominant individuals, known as gamergates.
Not only does this new caste of individuals exhibit a behavioural transition, but they also develop reproductive capabilities comparable to the queen; experience a five-fold extension in lifespan; and undergo neurohormonal, genetic and cellular changes.
Given that most social insects cannot change their caste, what determines this exceptional functional plasticity in H. saltator?
In a recently-published study, a group of researchers at the University of Pennsylvania set out to determine the molecular and genetic mechanisms responsible for this unique metamorphosis.
Results of their study revealed a notable dichotomy between the social castes and the hormonal pathways acting in the individuals of the caste.
In particular, two hormones: juvenile hormone III (JH3) and 20-hydroxyecdysone (20E), were identified as hallmarks of caste-specific gene expression in workers and gamergates respectively.
The crucial role of these hormones in determining the distinct caste-specific behavioural repertoires were proven when artificial delivery of JH3 to 10-day-old H. saltator individuals resulted in a population of worker-like individuals, with caste status being confirmed genetically. Similarly, delivery of 20E resulted in a population of queen-like individuals.
To gain a more profound understanding of this differential gene expression between castes and the molecular ‘switch’ driving the transition, the group cultured neurones from H. saltator and added each of the hormones. This identified a molecule activated by both hormones, known as Krüppel homolog 1 (Kr-h1) which was found to bind to the promoters of genes to repress their transcription.
Furthermore, they discovered that JH3 and 20E induce Kr-h1 to downregulate, or essentially ‘turn off’, gamergate-biased genes in workers and worker-biased genes in gamergates. In other words, ‘socially inappropriate’ gene expression patterns are repressed in a caste-specific manner, enabling socially-regulated and distinct brain states to be achieved in each group.
For example, removal of Kr-h1 via knockout mutation in gamergates was found to promote hunting — a behaviour characteristic of the worker caste which is therefore usually repressed.
Interestingly, Kr-h1 had previously been identified as an effector of JH3, but its involvement with 20E determined by this study was novel. Upon examination of Kr-h1 distribution in the Harpegnathos saltator genome, it was determined Kr-h1 acts via binding to, and causing a change in the structure of chromatin (the DNA-protein complex chromosomes are composed of), specifically in the brain.
Attempting to determine the way in which this singular transcription factor can result in caste-specific chromatin profiles proved more challenging. One hypothesis postulated that two variations, known as isoforms, of the Kr-h1 protein exist, with JH3 and 20E acting to induce different isoforms.
Another hypothesised the complexing of Met and EcR (two nuclear receptors of JH3 and 20E) with Kr-h1 may be responsible. This builds upon the idea that the differential hormone specificity between JH3 and 20E means that Kr-h1 can be recruited to different genes depending on the caste of the individual.
The researchers noted that the two hypothesised mechanisms in caste-specific Kr-h1 action need not be mutually exclusive, but rather the most probable explanation combines the two: different isoforms may be recruited to different genes by different associated proteins.
Whilst the interplay between EcR, Met and Kr-h1 requires further research, the pronounced behavioural differences observed in Harpegnathos saltator have provided an exceptional model system for scientists to begin to determine how social experiences lead to the establishment of enduring patterns of behaviour via molecular regulation.
Furthermore, the evolutionary significance of this research is profound as JH3 and 20E have been identified in multiple gene expression signatures of several other social insect species, meaning that Kr-h1 caste maintenance may also be a conserved mechanism in arthropods.
Given that behavioural plasticity is crucial in the survival of many phyla of life, an ever-expanding understanding of the molecular mechanisms underpinning this phenomenon will continue to offer a more comprehensive classification of factors facilitating survival success, not only in social insects, but in many animals beyond.
Illustration: Verity Laycock