Unravelling the Evolution of the Allatostatin-Type A, KISS and Galanin Peptide-Receptor Gene Families in Bilaterians: Insights from Anopheles Mosquitoes

Abstract

Allatostatin type A receptors (AST-ARs) are a group of G-protein coupled receptors activated by members of the FGL-amide (AST-A) peptide family that inhibit food intake and development in arthropods. Despite their physiological importance the evolution of the AST-A system is poorly described and relatively few receptors have been isolated and functionally characterised in insects. The present study provides a comprehensive analysis of the origin and comparative evolution of the AST-A system. To determine how evolution and feeding modified the function of AST-AR the duplicate receptors in Anopheles mosquitoes, were characterised. Phylogeny and gene synteny suggested that invertebrate AST-A receptors and peptide genes shared a common evolutionary origin with KISS/GAL receptors and ligands. AST-ARs and KISSR emerged from a common gene ancestor after the divergence of GALRs in the bilaterian genome. In arthropods, the AST-A system evolved through lineage-specific events and the maintenance of two receptors in the flies and mosquitoes (Diptera) was the result of a gene duplication event. Speciation of Anopheles mosquitoes affected receptor gene organisation and characterisation of AST-AR duplicates (GPRALS1 and 2) revealed that in common with other insects, the mosquito receptors were activated by insect AST-A peptides and the iCa2+-signalling pathway was stimulated. GPRALS1 and 2 were expressed mainly in mosquito midgut and ovaries and transcript abundance of both receptors was modified by feeding. A blood meal strongly up-regulated expression of both GPRALS in the midgut (p < 0.05) compared to glucose fed females. Based on the results we hypothesise that the AST-A system in insects shared a common origin with the vertebrate KISS system and may also share a common function as an integrator of metabolism and reproduction. Highlights: AST-A and KISS/GAL receptors and ligands shared common ancestry prior to the protostome-deuterostome divergence. Phylogeny and gene synteny revealed that AST-AR and KISSR emerged after GALR gene divergence. AST-AR genes were present in the hemichordates but were lost from the chordates. In protostomes, AST-ARs persisted and evolved through lineage-specific events and duplicated in the arthropod radiation. Diptera acquired and maintained functionally divergent duplicate AST-AR genes.

Honey Bee Allatostatins Target Galanin/Somatostatin-Like Receptors and Modulate Learning: A Conserved Function?

“…As our phylogenetic analysis confirms, Apime-ASTA-R and Apime-ASTC-R belong to two distinct receptor families that include, respectively, mammalian galanin and somatostatin receptors [ 19 , 50 , 96 – 98 ]. Yet, as is often the case for small neuropeptides, this conservation does not fully apply to the ligands.…”

AstA Signaling Functions as an Evolutionary Conserved Mechanism Timing Juvenile to Adult Transition

“…However, a comprehensive evolutionary study of the AstA receptor 1 gene revealed that it shares an evolutionary ancestor gene with the mammalian GPR54 receptor gene [41]. Moreover, the Drosophila AstA peptide and the human KISS peptide share a conserved FGL motif, suggesting that AstA and KISS could originate from a common ancestor [41]. As previously mentioned, the KISS/GPR54 pathway promotes pulsatile secretion of GnRH, a necessary event for steroid production and sexual maturation in vertebrates [42].…”

“…AstA was initially described as an arthropod-specific hormone inhibiting food intake and juvenile hormone (JH) secretion [40]. However, a comprehensive evolutionary study of the AstA receptor 1 gene revealed that it shares an evolutionary ancestor gene with the mammalian GPR54 receptor gene [41]. Moreover, the Drosophila AstA peptide and the human KISS peptide share a conserved FGL motif, suggesting that AstA and KISS could originate from a common ancestor [41].…”

Peptide Hormones in the Insect Midgut

“…The C-terminus of allatostatin type A (AST-A) is a conserved FGL amine motif, which can be detected in the brain and midgut of insects; its receptor is a G protein-coupled receptor. AST-A peptide, which can inhibit the secretion of JH, can also regulate food intake through inhibition or reduction of food intake (Felix et al, 2015). After Anopheles mosquitoes sucked blood, the expression levels of AST-A receptor genes GPRALS1 and 2 in the midgut were significantly higher than after the mosquitoes ingested glucose, however, these expression levels were reduced in the head and ovary (Felix et al, 2015).…”