Oxytocin-like signaling in ants influences metabolic gene expression and locomotor activity

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Abstract

<p class="first" id="P1">Ants are emerging model systems to study cellular signaling because distinct castes possess different physiologic phenotypes within the same colony. Here we studied the functionality of inotocin signaling, an insect ortholog of mammalian oxytocin (OT), which was recently discovered in ants. In <i>Lasius</i> ants, we determined that specialization within the colony, seasonal factors, and physiologic conditions down-regulated the expression of the OT-like signaling system. Given this natural variation, we interrogated its function using RNAi knockdowns. Next-generation RNA sequencing of OT-like precursor knock-down ants highlighted its role in the regulation of genes involved in metabolism. Knock-down ants exhibited higher walking activity and increased self-grooming in the brood chamber. We propose that OT-like signaling in ants is important for regulating metabolic processes and locomotion. </p>

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Oxytocin, vasopressin, and the neurogenetics of sociality.

Zoe R. Donaldson, Larry J Young (2008)

There is growing evidence that the neuropeptides oxytocin and vasopressin modulate complex social behavior and social cognition. These ancient neuropeptides display a marked conservation in gene structure and expression, yet diversity in the genetic regulation of their receptors seems to underlie natural variation in social behavior, both between and within species. Human studies are beginning to explore the roles of these neuropeptides in social cognition and behavior and suggest that variation in the genes encoding their receptors may contribute to variation in human social behavior by altering brain function. Understanding the neurobiology and neurogenetics of social cognition and behavior has important implications, both clinically and for society.

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Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance.

Joshua McElwee, Eugene Schuster, Eric Blanc … (2004)

In the nematode Caenorhabditis elegans, formation of the long-lived dauer larva and adult aging are both controlled by insulin/insulin-like growth factor-1 signaling. Potentially, increased adult life span in daf-2 insulin/insulin-like growth factor-1 receptor mutants results from mis-expression in the adult of a dauer larva longevity program. By using oligonucleotide microarray analysis, we identified a dauer transcriptional signature in daf-2 mutant adults. By means of a nonbiased statistical approach, we identified gene classes whose expression is altered similarly in dauers and daf-2 mutants, which represent potential determinants of life span. These include known determinants of longevity; the small heat shock protein/alpha-crystallins are up-regulated in both milieus. The cytochrome P450, short-chain dehydrogenase/reductase, UDP-glucuronosyltransferase, and glutathione S-transferase (in daf-2 mutants) gene classes were also up-regulated. These four gene classes act together in metabolism and excretion of toxic endobiotic and xenobiotic metabolites. This suggests that diverse toxic lipophilic and electrophilic metabolites, disposed of by phase 1 and phase 2 drug metabolism, may be the major determinants of the molecular damage that causes aging. In addition, we observed down-regulation of genes linked to nutrient uptake, including nhx-2 and pep-2. These work together in the uptake of dipeptides in the intestine, implying dietary restriction in daf-2 mutants. Some gene groups up-regulated in dauers and/or daf-2 were enriched for certain promoter elements as follows: the daf-16-binding element, the heat shock-response element, the heat shock-associated sequence, or the hif-1-response element. By contrast, the daf-16-associated element was enriched in genes down-regulated in dauers and daf-2 mutants. Thus, particular promoter elements appear longevity-associated or aging associated.

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Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

Daniel F. Simola, Lothar Wissler, Greg Donahue … (2013)

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor–binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb ) and trans (e.g., fork head ) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila . Thus, while the “socio-genomes” of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.

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Author and article information

Journal

Title: The FASEB Journal

Abbreviated Title: The FASEB Journal

Publisher: FASEB

ISSN (Print): 0892-6638

ISSN (Electronic): 1530-6860

Publication date Created: December 2018

Publication date (Print): December 2018

Volume: 32

Issue: 12

Pages: 6808-6821

Affiliations

[1 ]Center for Physiology and Pharmacology, Medical University of Vienna, Vienna, Austria;

[2 ]Division of Computational Systems Biology (CUBE), Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria;

[3 ]Ludwig Boltzmann Institute for Cancer Research, Vienna, Austria;

[4 ]Institute of Science and Technology (IST) Austria, Klosterneuburg, Austria;

[5 ]Institute for Molecular Biosciences, The University of Queensland, St. Lucia, Queensland, Australia; and

[6 ]Faculty of Chemistry, Institute of Biological Chemistry, University of Vienna, Vienna, Austria

Article

DOI: 10.1096/fj.201800443

PMC ID: 6174076

PubMed ID: 29939785

SO-VID: 06cbc103-2148-4b31-94ff-0e1718dacc06

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Oxytocin-like signaling in ants influences metabolic gene expression and locomotor activity

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Most cited references 48

Oxytocin, vasopressin, and the neurogenetics of sociality.

Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance.

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

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