Sexual plasticity: A fishy tale

Abstract

SUMMARYTeleost fish exhibit remarkably diverse and plastic patterns of sexual development. One of the most fascinating modes of plasticity is functional sex change, which is widespread in marine fish including species of commercial importance; however, the regulatory mechanisms remain elusive. In this review, we explore such sexual plasticity in fish, using the bluehead wrasse (Thalassoma bifasciatum) as the primary model. Synthesizing current knowledge, we propose that cortisol and key neurochemicals modulate gonadotropin releasing hormone and luteinizing hormone signaling to promote socially controlled sex change in protogynous fish. Future largescale genomic analyses and systematic comparisons among species, combined with manipulation studies, will likely uncover the common and unique pathways governing this astonishing transformation. Revealing the molecular and neuroendocrine mechanisms underlying sex change in fish will greatly enhance our understanding of vertebrate sex determination and differentiation as well as phenotypic plasticity in response to environmental influences.

Bending Genders: The Biology of Natural Sex Change in Fish

“…Detailed histological descriptions of gonadal sex change have been made for numerous species representative of protandrous [Godwin, 1994;Guiguen et al, 1994; reviewed by Lee et al, 2001;Wu et al, 2010a], protogynous [Nakamura et al, 1989;Lo Nostro et al, 2003;Muncaster et al, 2013; reviewed by Liu et al, 2016], and bidirectional ; reviewed by Cole, 2010Cole, , 2011Kuwamura et al, 2015] hermaphrodites. There is considerable diversity in gonadal configuration and ontogeny among different sequentially hermaphroditic lineages, which closely follows phylogenetic lines and reflects the multiple independent evolutionary origins of hermaphroditism [Sadovy de Mitcheson and Liu, 2008;Cole, 2010].…”

“…In protogynous hermaphrodites, early male tissues are usually first observed at the periphery of the ovarian lamellae in the vicinity of the germinal epithelium [Lo Nostro et al, 2003]. However, it is difficult to establish whether proliferating spermatogonia arise from a dormant, but sexually differentiated, germ cell population (i.e., co-existence of oogonia and spermatogonia) or from sexually bipotent primordial germ cells that are undifferentiated or even reprogrammable [Lo Nostro et al, 2003;Liu et al, 2016].…”

“…However, the precise roles of GnRH and GtH signalling in controlling sex change is difficult to model as patterns are inconsistent even between closely related species, e.g., contradictory patterns of expression for GtH receptors are observed in protogynous grouper [Alam et al, 2010;Hu et al, 2011] and may reflect species-specific gonadotropin functioning in teleosts [Levavi-Sivan et al, 2010]. The perception and processing of external cues into the physiological responses that characterise sex change remain poorly understood but have been investigated most intensively in socially protogynous wrasses [see recent review by Lamm et al, 2015;Liu et al, 2016]. Rapid neurochemical changes in the brain drive behavioural sex change and precede gonadal restructuring, which is coordinated via the HPG axis, by several days [Larson 2003a, b;Semsar and Godwin, 2003; reviewed by Godwin and Thompson, 2012;Lamm et al, 2015].…”

“…IT, the teleost homologue of mammalian oxytocin, is also associated with social status and sex-specific reproductive behaviours [Goodson and Bass, 2000;Lema et al, 2015]. These are of interest, as rank may serve as a primer for sex change in socially polygynous breeders Liu et al, 2016]. In a recent whole-transcriptome analysis of bluehead wrasse forebrain, increased expression of the gene encoding IT was one of the few statistically significant changes detected across sex change [Liu, 2016].…”

Is gender just a category? The two‐plus sex advantage

“…gastropods [Collin, 2013]) or in social structure (e.g. clown fi sh [Casas et al, 2016], bluehead wrasse [Warner and Swearer, 1991;Liu et al, 2017]). …”