Abstract
Sexual fate was once considered an immutable process determined during early embryonic development. However, sexual determination can be dynamic; many species, especially among teleost fishes, display striking sexual plasticity, with the capacity to change their sexual phenotype during their lifetime. Natural sex change involves coordinated transformations in behavior, morphology, and neuroendocrine and molecular pathways. Although social dominance is pivotal in initiating sex change, as it determines which individual within a group will transition, our understanding of how dominance hierarchies form in such systems remains limited.
In this thesis, I examine hierarchy formation in female New Zealand spotty wrasse (𝘕𝘰𝘵𝘰𝘭𝘢𝘣𝘳𝘶𝘴 𝘤𝘦𝘭𝘪𝘥𝘰𝘵𝘶𝘴; referred to as “spotty”), combining behavioral observations with analyses of neural activation following social disruption. I show that size-based linear hierarchies quickly formed and that social disruption of established hierarchies induced rapid behavioral changes, particularly in second-ranked fish, which readily assumed dominance in the absence of the first-ranked fish. Neural activation analyses revealed that areas associated with the social decision-making network had increased activation in second-ranked fish following removal of the dominant fish. These findings shed light on the neurobehavioral basis of social dominance and provide a foundation for exploring the cellular and molecular mechanisms that mediate socially regulated sex change.
To further investigate the behavioral mechanisms shaping hierarchies, I tested for winner–loser effects. Spotty with prior losing experiences were more likely to lose subsequent size-matched contests, demonstrating a clear loser effect, whereas no evidence for a winner effect emerged. Individual aggression, assessed with a mirror test before and after fights, correlated positively with subsequent aggression and submissive displays in losers, but these traits did not predict outcomes. Significant shifts in aggression following contests occurred only in individuals that drew their final size-matched fight. A repeated round of contests one week later failed to replicate winner–loser patterns, with only drawn fights again eliciting changes in aggression. Across both sessions, aggression displayed low to moderate repeatability. These results highlight the presence of loser effects in this species while also emphasizing the temporal variability of contest outcomes and the behavioral complexity underlying hierarchy formation.
Finally, I investigated potential cognitive mechanisms that may facilitate hierarchy assessment. Because direct interactions with every group member can be energetically costly, individuals may rely on complex cognitive processes, such as transitive inference (TI), to infer social relationships. TI enables individuals to deduce unknown dominance relationships (e.g., if A > B and B > C, then A > C) and has been demonstrated across a wide range of taxa, from vertebrates to invertebrates. Spotty did not demonstrate TI from observation alone. Rather, direct interactions might be necessary for transitive thinking to occur in spotty. TI could also not be ecologically relevant for spotty, with other behavioral mechanisms being better suited for hierarchy formation.
Overall, this thesis provides new insights into the behaviors of sex-changing fish, exploring mechanisms of hierarchy formation that have previously been understudied in sequential hermaphrodites and largely overlooked in females. These findings lay important groundwork for future research investigating what behavioral mechanisms assist in dominance hierarchy formation and how social environments cue and prime individuals for sex change.