Reproductive roles of the vasopressin/oxytocin neuropeptide family in teleost fishes

Abstract

The vertebrate nonapeptide families arginine vasopressin (AVP) and oxytocin (OXT) are considered to have evolved from a single vasopressin-like peptide present in invertebrates and termed arginine vasotocin in early vertebrate evolution. Unprecedented genome sequence availability has more recently allowed new insight into the evolution of nonapeptides and especially their receptor families in the context of whole genome duplications. In bony fish, nonapeptide homologues of AVP termed arginine vasotocin (Avp) and an OXT family peptide (Oxt) originally termed isotocin have been characterized. While reproductive roles of both nonapeptide families have historically been studied in several vertebrates, their roles in teleost reproduction remain much less understood. Taking advantage of novel genome resources and associated technological advances such as genetic modifications in fish models, we here critically review the current state of knowledge regarding the roles of nonapeptide systems in teleost reproduction. We further discuss sources of plasticity of the conserved nonapeptide systems in the context of diverse reproductive phenotypes observed in teleost fishes. Given the dual roles of preoptic area (POA) synthesized Avp and Oxt as neuromodulators and endocrine/paracrine factors, we focus on known roles of both peptides on reproductive behaviour and the regulation of the hypothalamic-pituitary-gonadal axis. Emphasis is placed on the identification of a gonadal nonapeptide system that plays critical roles in both steroidogenesis and gamete maturation. We conclude by highlighting key research gaps including a call for translational studies linking new mechanistic understanding of nonapeptide regulated physiology in the context of aquaculture, conservation biology and ecotoxicology.

Keywords: courtship behaviour; endocrine system; hormone; hypothalamic–pituitary–gonadal axis; isotocin; neuromodulator; paracrine; vasotocin.

Figure 1

Tissue-specific expression profiles of nonapeptide precursor coding genes in spotted gar (A), rainbow trout, Oncorhynchus mykiss (B), and brook trout, Salvelinus fontinalis (C) derived from the Phylofish RNA-seq database (www.phylofish.signae.org) queried on June 1^st, 2022 (20).

Figure 2

Presence of avpr1 (A), avpr2/avpr2l (B) and oxtr (C) genes in published fish genomes accessed on NCBI (www.pubmed.com) on June 1^st, 2022.

Figure 3

Microsynteny analysis (A), predicted AA sequence alignment (B) and RNA-seq based tissue expression profiles (C) of oxtra and oxtrb paralogues in select teleost fishes. Micro-synteny analysis of oxtr paralogue gene loci was manually conducted on NCBI (www.pubmed.com) derived genome sequences retrieved on June 1^st, 2022, while oxtr gene paralogue sequence-predicted AA sequences were aligned using Clustal Omega (https://www.ebi.ac.uk/Tools/msa/clustalo/). RNA-seq based tissue expression profiles of oxtr paralogues was created derived from the Phylofish RNA-seq database queried on June 1^st, 2022 (20).

Figure 4

Schematic representation of mechanistic knowledge of nonapeptide roles in teleost reproduction. The Avp system is highlighted in yellow, while the Oxt system is represented in blue. Circled nonapeptides indicate sites of synthesis, while connecting lines represent neuronal, endocrine, and paracrine pathways. Specific receptor involvement in regulatory function of HPG axis components is symbolized as defined in Figure 2 .