Neuroendocrinology of sexual plasticity in teleost fishes

Abstract

The study of sex differences has produced major insights into the organization of animal phenotypes and the regulatory mechanisms generating phenotypic variation from similar genetic templates. Teleost fishes display the greatest diversity of sexual expression among vertebrate animals. This diversity appears to arise from diversity in the timing of sex determination and less functional interdependence among the components of sexuality relative to tetrapod vertebrates. Teleost model systems therefore provide powerful models for understanding gonadal and non-gonadal influences on behavioral and physiological variation. This review addresses socially-controlled sex change and alternate male phenotypes in fishes. These sexual patterns are informative natural experiments that illustrate how variation in conserved neuroendocrine pathways can give rise to a wide range of reproductive adaptations. Key regulatory factors underlying sex change and alternative male phenotypes that have been identified to date include steroid hormones and the neuropeptides GnRH and arginine vasotocin, but genomic approaches are now implicating a diversity of other influences as well.

Figure 1

Diversity of sexual patterns in fishes for both gonochoristic and hermaphroditic species. ‘AMP’ refers to alternate male phenotypes.

Figure 2

Steroid hormone levels in plasma of the saddleback wrasse (Thalassoma duperrey) shown for natural females and TP males and in females induced to undergo sex change in experimental pens (Redrawn from Nakamura et al., 2005). Stages in blue box indicate progress in sex change process when samples were taken.

Figure 3

Steroid hormone levels in plasma of the anemonefish Amphiprion melanopus for breeding males and females captured from unmanipulated social groups as well as males undergoing protandrous sex change induced by removing dominant females from social groups. Relative levels of different hormones are depicted to approximately the same scale except for cortisol, where levels were substantially higher. (Redrawn from Godwin and Thomas, 1993).

Figure 4

Social status influences AVT mRNA levels in the preoptic area of the hypothalamus in bluehead wrasses while gonadal status does not. Dominant individuals were the largest in their social groups while subordinants were not. Intact animals underwent ‘sham’ operations to control for the surgical procedure. Inset shows AVT mRNA in the preoptic area visualized by the technique of in situ hybridization. Figure depicts relative AVT mRNA levels in this comparison from Semsar and Godwin (2003).

Figure 5

Comparisons possible across sexual phenotypes in species with AMPs. Notes beside arrows indicate factors that are being varied or held ‘constant’ in each comparison.

Figure 6

Ontogeny of alternative male phenotypes in the bluegill sunfish, Lepomis macrochirus. Numbers reflect age in years and gray fill in lines indicates approximate timing of sexual maturity (figure is from Neff and Knapp, 2009 with permission).