Arginine Vasotocin, Isotocin and Nonapeptide Receptor Gene Expression Link to Social Status and Aggression in Sex‐Dependent Patterns

Abstract

Nonapeptide hormones of the vasopressin/oxytocin family regulate social behaviours. In mammals and birds, variation in behaviour also is linked to expression patterns of the V1a-type receptor and the oxytocin/mesotocin receptor in the brain. Genome duplications, however, expand the diversity of nonapeptide receptors in actinopterygian fishes, and two distinct V1a-type receptors (v1a1 and v1a2) for vasotocin, as well as at least two V2-type receptors (v2a and v2b), have been identified in these taxa. The present study investigates how aggression connected to social status relates to the abundance patterns of gene transcripts encoding four vasotocin receptors, an isotocin receptor (itr), pro-vasotocin (proVT) and pro-isotocin (proIT) in the brain of the pupfish Cyprinodon nevadensis amargosae. Sexually-mature pupfish were maintained in mixed-sex social groups and assessed for individual variation in aggressive behaviours. Males in these groups behaved more aggressively than females, and larger fish exhibited higher aggression relative to smaller fish of the same sex. Hypothalamic proVT transcript abundance was elevated in dominant males compared to subordinate males, and correlated positively with individual variation in aggression in both social classes. Transcripts encoding vasotocin receptor v1a1 were at higher levels in the telencephalon and hypothalamus of socially subordinate males than dominant males. Dominant males exhibited elevated hypothalamic v1a2 receptor transcript abundance relative to subordinate males and females, and telencephalic v1a2 mRNA abundance in dominant males was also associated positively with individual aggressiveness. Transcripts in the telencephalon encoding itr were elevated in females relative to males, and both telencephalic proIT and hypothalamic itr transcript abundance varied with female social status. Taken together, these data link hypothalamic proVT expression to aggression and implicate forebrain expression of the V1a-type receptor v1a2 as potentially mediating the effects of vasotocin on behaviour in male fish. These findings also illustrate how associations between social status, aggression and gene expression within the VT and IT nonapeptide systems can be contingent on behavioural context.

Peer Review #2 of "Conservation and diversity in expression of candidate genes regulating socially-induced female-male sex change in wrasses (v0.1)"

“…Brain gene expression patterns are highly heterogeneous and it remains possible that localised cyp19a1b expression changes are important, but would not be detected in studies at a whole brain or fore/midbrain level. Our data supports the role isotocin plays in modulating teleost socio-sexual behaviours, and social dominance hierarchies in particular [32,82,83]. In bluehead wrasse, it expression is TP male biased and upregulated across sex change, beginning with a median 2-fold increase at stage 1 when behavioural changes first occur.…”

Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks

“…The vasoactive intestinal peptide receptor 1b was differentially expressed between aggressive and nonaggressive sticklebacks in both brainstem and cerebellum, although interestingly in opposite directions in the two brain regions. Arginine vasopressin and its receptors are other important molecules involved in social behaviour in vertebrates (Filby et al, 2010; Santangelo & Bass, 2010; Oldfield & Hofmann, 2011; Godwin & Thompson, 2012; Huffman et al, 2015; Lema et al, 2015; Oldfield et al, 2015; Yokoi et al, 2015), including sticklebacks (Kleszczynska et al, 2012). The arginine vasotocin receptor 2a was downregulated in aggressive individuals in brainstem, although several studies have pointed to the importance of the V1a receptor in fishes, e.g.…”

Sexual plasticity: A fishy tale

“…AVT is a key mediator of social and sexual behaviors in fish (reviewed by Godwin and Thompson, ), and plays a critical role in stimulating behavioral sex change in bluehead wrasses (Semsar et al, ; Semsar and Godwin, , ). Isotocin is associated with social and sexual behaviors in fish (Lema et al, ), but its role in sex change remains largely unknown (reviewed by Godwin and Thompson, ; Lamm et al, ). Kisspeptins were recently suggested to directly mediate AVT‐ and isotocin‐producing neurons in medaka (Kanda et al, ), but how remains unclear.…”