Social influences on the arginine vasotocin system are independent of gonads in a sex-changing fish

Abstract

Many neuropeptide systems subserving sex-typical behavior are dependent on sex steroids for both their organization early in life and activation during maturity. The arginine vasopressin/vasotocin (AVP/AVT) system is strongly androgen dependent in many species and critically mediates responses to sociosexual stimuli. The bluehead wrasse is a teleost fish that exhibits a female-to-male sex change in response to social cues, and neither the development nor the maintenance of male-typical behavior depends on the presence of gonads. To examine social and gonadal inputs on the AVP/AVT system in the preoptic area (POA) of the hypothalamus, we conducted three field experiments. In the first experiment, we found that AVT mRNA abundance is higher in sex-changing females that attain social dominance and display dominant male behavior than in subordinate females, regardless of whether the dominant females were intact or ovariectomized. However, AVT-immunoreactive (IR) soma size in the gigantocellular POA (gPOA), but not in the magnocellular or parvocellular POA, increased only when females were displaying both dominant male behavior and had developed testes. In the second experiment, castration of dominant terminal-phase males had no effect on AVT mRNA abundance or any behavior we measured but did increase gPOA AVT-IR soma size compared with sham-operated controls. In the third experiment, 11-ketotestosterone implants in socially subordinate, ovariectomized females had no effect on either AVT mRNA abundance or AVT-IR soma size compared with controls. These results demonstrate that the AVT neural phenotype in the bluehead wrasse can be strongly influenced by social status, and that these social influences can be manifested independent of gonads.

Figure 1.

A–C, Photomicrographs of AVT-IR neurons in the gPOA (A), mPOA (B), and pPOA (C). D, Mean ± SEM average AVT-IR soma sizes for TP males within each region of the POA. Sample sizes are indicated within bars. Scale bars, 100 μm.

Figure 2.

AVT neural phenotype from females in experiment 1. A, AVT mRNA hybridization signal (mean ± SEM, standardized by body size). B, Mean ± SEM average AVT-IR soma cross-sectional area in the three POA regions. Sample sizes are indicated within the bars, and asterisks indicate significant differences among treatment groups (within POA regions in B).

Figure 3.

AVT neural phenotype from sham-operated and castrated TP males in experiment 2. A, AVT mRNA hybridization signal (mean ± SEM, standardized by body size) from 2000 and 2001. B, Mean ± SEM average AVT-IR soma cross-sectional area in the three POA regions. Sample sizes are indicated within the bars, and asterisks indicate significant differences among treatment groups (within POA regions in B).

Figure 4.

AVT neural phenotype from oil- and 11KT-treated females in experiment 3. A, AVT mRNA hybridization signal (mean ± SEM, standardized by body size). B, Mean ± SEM average AVT-IR soma cross-sectional area in the three POA regions. Sample sizes are indicated within the bars.