Epigenetic Regulator CoREST Controls Social Behavior in Brain of Ants

Eusocial insects (showing an advanced level of social organization, in which a single female produces offspring, and nonreproductive individuals cooperate in caring for the young) are among the most successful taxa (taxonomic group such as a species, family, or class) on Earth, because of their ability to segregate tasks among different (often morphologically or behaviorally distinct) individuals within a colony. Because of this extreme phenotypic and behavioral plasticity, ants have emerged as experimental models for asking questions about complex social behavior and investigating epigenetic mechanisms that program expression of the same genome into disparate individual phenotypes. An important example of this “division of labor” involves differentiation of individuals into sterile (worker) and reproductive (queen) physiological castes. Another striking manifestation — in many eusocial insect species — is the allocation of distinct colony roles among worker groups.

Often summarized in these GEITP pages: Multifactorial traits in animals involve genetic (DNA sequence) differences, epigenetic factors, environmental effects, endogenous influences, and contributions from the microbiome. Epigenetic alterations (chromosomal manifestations that are not caused by DNA sequence differences) are associated with differential morphology and behavior among ant castes — involving distinct patterns of chromatin modifications including histone posttranslational modifications (hPTMs) and possibly DNA methylation. hPTMs result in a diverse set of epigenetic signals that typically occur on histone-protein N-terminal amino acid tails and alter transcription, via several mechanisms.

Another emerging mediator of caste division of labor — in multiple eusocial insects — is the metamorphosis-associated hormones, juvenile hormone (JH) and ecdysone (20E). These small-molecule hormones play important roles in both the developmental and behavioral division of labor. The Florida carpenter ant, Camponotus floridanus, has two distinct worker castes: Major and Minor workers. These worker castes display diverse morphology and behavior: the smaller Minor workers perform foraging and nursing of brood; the larger Major workers defend the nest as soldiers and very rarely forage.

Authors [see attached article] discovered that innate chromatin regulation via the corepressor for element-1-silencing transcription (CoREST) factor mediates the natural programming of foraging behavior in Minor workers; moreover, reprogramming of Major workers to forage uses this same CoREST epigenetic pathway. Authors found that CoREST is upregulated, upon reprogramming,

and is required for the epigenetic switch to foraging. CoREST was shown to repress expression of enzymes that degrade JH, a hormone that is elevated upon reprogramming. High CoREST levels, low JH-degrader expression, and high JH levels are seen in natural Minor workers, revealing parallel mechanisms of natural vs reprogrammed foraging. These data demonstrate chromatin regulation via CoREST is a central process to programming of ant social behavior, and these results have potential implications for other manifestations of behavioral epigenetics. 😊

DwN

Mol Cell Jan 2020; 77: 1-14

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