An evolutionarily conserved pathway mediated by neuroparsin-A regulates reproductive plasticity in ants.

Phenotypic plasticity displayed by an animal in response to different environmental conditions is supposedly crucial for its survival and reproduction. The female adults of some ant lineages display phenotypic plasticity related to reproductive role. In pharaoh ant queens, insemination induces substantial physiological/behavioral changes and implicates remarkable gene regulatory network (GRN) shift in the brain. Here, we report a neuropeptide neuroparsin A (NPA) showing a conserved expression pattern associated with reproductive activity across ant species. Knock-down of NPA in unmated queen enhances ovary activity, whereas injection of NPA peptide in fertilized queen suppresses ovary activity. We found that NPA mainly affected the downstream gene JHBP in the ovary, which is positively regulated by NPA and suppression of which induces elevated ovary activity, and shadow which is negatively regulated by NPA. Furthermore, we show that NPA was also employed into the brain-ovary axis in regulating the worker reproductive changes in other distantly related species, such as Harpegnathos venator ants.

On the origin and evolution of RNA editing in metazoans.

Extensive adenosine-to-inosine (A-to-I) editing of nuclear-transcribed mRNAs is the hallmark of metazoan transcriptional regulation. Here, by profiling the RNA editomes of 22 species that cover major groups of Holozoa, we provide substantial evidence supporting A-to-I mRNA editing as a regulatory innovation originating in the last common ancestor of extant metazoans. This ancient biochemistry process is preserved in most extant metazoan phyla and primarily targets endogenous double-stranded RNA (dsRNA) formed by evolutionarily young repeats. We also find intermolecular pairing of sense-antisense transcripts as an important mechanism for forming dsRNA substrates for A-to-I editing in some but not all lineages. Likewise, recoding editing is rarely shared across lineages but preferentially targets genes involved in neural and cytoskeleton systems in bilaterians. We conclude that metazoan A-to-I editing might first emerge as a safeguard mechanism against repeat-derived dsRNA and was later co-opted into diverse biological processes due to its mutagenic nature.

A single-cell transcriptomic atlas tracking the neural basis of division of labour in an ant superorganism.

Ant colonies with permanent division of labour between castes and highly distinct roles of the sexes have been conceptualized to be superorganisms, but the cellular and molecular mechanisms that mediate caste/sex-specific behavioural specialization have remained obscure. Here we characterized the brain cell repertoire of queens, gynes (virgin queens), workers and males of Monomorium pharaonis by obtaining 206,367 single-nucleus transcriptomes. In contrast to Drosophila, the mushroom body Kenyon cells are abundant in ants and display a high diversity with most subtypes being enriched in worker brains, the evolutionarily derived caste. Male brains are as specialized as worker brains but with opposite trends in cell composition with higher abundances of all optic lobe neuronal subtypes, while the composition of gyne and queen brains remained generalized, reminiscent of solitary ancestors. Role differentiation from virgin gynes to inseminated queens induces abundance changes in roughly 35% of cell types, indicating active neurogenesis and/or programmed cell death during this transition. We also identified insemination-induced cell changes probably associated with the longevity and fecundity of the reproductive caste, including increases of ensheathing glia and a population of dopamine-regulated Dh31-expressing neurons. We conclude that permanent caste differentiation and extreme sex-differentiation induced major changes in the neural circuitry of ants.