Socially Influenced Sex Change in Anemonefishes


The clownfish or anemonefish, Amphiprion ocellaris, typically live most of their life on or in very close proximity to a sea anemone in small groups from 3 up to 6 or 7 depending on the size of the anemone. In these groups, the largest is always the reproductive female, the second largest, the male and the smaller individuals are undifferentiated. If the female is removed, the male will transform into a reproductive female over a period of months to years. The process starts by the male establishing social dominance in the group.  Next, within 6 months, the parts of the brain that control the gonads change to the female form in terms of cellular composition.  During this brain transformation, body size grows considerably, but the gonads regress to containing a small number of undeveloped eggs and very little testicular tissue which release male-typical sex steroids.  By 6 months, after the brain changes are completed, the “male” behaves as a female.  By that we mean he/she is the primary defender of the territory, and does little care of the eggs if they are introduced, which is typical of the natural history of the species.  In addition, the sex-changing fish is recognized by other fish as a female even though “his” gonads and sex steroids remain more male-like than female-like.  At some point, which could take a few years, the female’s brain sends the signal to the gonads to develop fully formed eggs, and she is ready to reproduce.  All the while this is happening, the largest of the undifferentiated fish becomes a male and the partner of the sex changing female.  If the male is removed instead of the female, the undifferentiated fish can take as little as 1 week before they are able to reproduce.  It is possible that some of these “undifferentiated” fish are actually males already,  just not currently reproducing because of behavioral suppression from the dominant reproductive pair.

The phenomenon of neuroplasticity is perhaps no better exemplified than in the anemonefishes and many other coral reef marine fishes which change sex depending on the outcome of territorial contests.  For the past 10 years, we have been maintaining a colony of Amphiprion ocellaris, a species of anemonefish easily kept and bred in the laboratory, to study sex differences in the brain and behavior, and the mechanisms by which the brain and behavior become feminized.   We have discovered that males are the primary care-givers of the eggs, that peptide neurotransmitters oxytocin and arginine vasotocin are crucially involved in shifting the males behavior between aggressively defending the nest from predators versus providing nurturing direct care to the eggs by fanning and nipping them.  Most recently we discovered that the non-breeders and male anemonefish will step-father eggs that are not their own, if given the opportunity.  Hence, anemonefish males have a fathering instinct, that needs only the egg stimulus and the opportunity for it to be displayed.   Recently, we published our first sex change paper, which documents the cellular changes in the preoptic area (part of the brain that controls the gonads and reproductive behavior) and gonads during sex change from male to female.  We discovered that as males change sex into females, their brains change first, sometimes long before their gonads.  Hence, anemonefish can exist with a female brain but male-like gonads and circulating sex steroids , questioning the way we define sex based on the gonads only.