The Need for Speed: Neuroendocrine Regulation of Socially-controlled Sex Change

Abstract

Socially-controlled functional sex change in fishes is a dramatic example of adaptive reproductive plasticity. Functional gonadal sex change can occur within a week while behavioral sex change can begin within minutes. Significant progress has been made in understanding the neuroendocrine bases of this phenomenon at both the gonadal and the neurobiological levels, but a detailed mechanistic understanding remains elusive. We are working with sex-changing wrasses to identify evolutionarily-conserved neuroendocrine pathways underlying this reproductive adaptation. One key model is the bluehead wrasse (Thalassoma bifasciatum), in which sex change is well studied at the behavioral, ecological, and neuroendocrine levels. Bluehead wrasses show rapid increases in aggressive and courtship behaviors with sex change that do not depend on the presence of gonads. The display of male-typical behavior is correlated with the expression of arginine vasotocin, and experiments support a role for this neuropeptide. Estrogen synthesis is also critical in the process. Female bluehead wrasses have higher abundance of aromatase mRNA in the brain and gonads, and estrogen implants block behavioral sex change. While established methods have advanced our understanding of sex change, a full understanding will require new approaches and perspectives. First, contributions of other neuroendocrine systems should be better characterized, particularly glucocorticoid and thyroid signaling. Second, advances in genomics for non-traditional model species should allow conserved mechanisms to be identified with a key next-step being manipulative tests of these mechanisms. Finally, advances in genomics now also allow study of the role of epigenetic modifications and other regulatory mechanisms in the dramatic alterations across the sex-change process.

Bending Genders: The Biology of Natural Sex Change in Fish

“…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].…”

“…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]. Crosstalk between these distinct, but likely overlapping, neuroendocrine pathways may mediate the effects of the social environment on gonadal state to coordinate sex change at the whole-body level.…”

“…Within minutes of TP male removal, dramatic neuroendocrine changes in the brain of large females elicit behavioural sex change [Godwin, 2010;Lamm et al, 2015]. These include fluctuations in several neurochemicals known to modulate social rank and sexually dimorphic reproductive behaviours in fishes and other vertebrates [Godwin et al, 2000;Perrault et al, 2003; reviewed by Godwin and Thompson, 2012].…”

“…The ecological and evolutionary contexts in which sequential hermaphroditism occurs in fishes are now well studied [reviewed by Nakamura et al, 2005;Avise and Mank, 2009;Godwin, 2009;Lamm et al, 2015]. The behavioural, anatomical, and hormonal transformations that characterise protogynous, protandrous, and bidirectional sex change are described for several representative species [e.g., Nakamura et al, 1989;Warner and Swearer, 1991;Godwin and Thomas, 1993].…”

The neuropeptide F/nitric oxide pathway is essential for shaping locomotor plasticity underlying locust phase transition

“…Typically, to maintain the required fission–fusion dynamics, swarming animals exhibit striking behavioral plasticity of different types (Snell-Rood, 2006; Szyf, 2010). Biochemical changes in the levels of neuromodulators, such as monoamines, neuropeptides, and neurohormones, are able to induce behavioral variation thus mediate behavioral plasticity (Freudenberg et al, 2015; Godwin et al, 2015; Zupanc and Lamprecht, 2000). Nevertheless, the molecular basis by which neural factors orchestrate behavioral plasticity in swarming animals is poorly understood in detail.…”