Transexual Fishes

Underwater Curacao

Teleost Fishes are the most sexually labile vertebrates, mammals the least. What I mean by sexual lability, is the capacity to become either a male or female, or both, depending on the circumstances. Moreover, this context-dependent sex extends well into adulthood.

Spanning that gap between fishes and mammals, in order of decreasing sexual lability, are amphibians, reptiles, and birds. I will explore the causes and implications of this trend in a later post. Here I will focus on one expression of sexual lability in fishes. It is important to remember that the process of sexual differentiation—the process through which females and males diverge—is highly conserved across all vertebrates, from fish to mammals, including the genes involved, the hormones, the relevant brain bits and the reproductive machinery.

Unbeknownst to most, many of the more common fishes you fill see in coral reefs are hermaphrodites. But a different kind of hermaphrodite than the hamlets discussed in the previous post. Hamlets are called simultaneous hermaphrodites, because they produce sperm and eggs at the same point in time. They are the kind of hermaphrodites we usually think of when we think about hermaphrodites. But there is another kind of hermaphroditism among fishes, one which is in fact much more common than hamlet style hermaphroditism. This more common kind of hermaphrodite spends part of its life as one sex, then changes to the other. They are called sequential hermaphrodites.

Sequential hermaphrodites come in two flavors: those that first reproduce as males, then transform into females later in life; and those that first reproduce as females and later transform into males. The male to female sex changers are called protandrous hermaphrodites (“pro”, short for “proto” = first, “androus”, as in androgen = male). Those that make the opposite transition, from female to male, are called protogynous (“proto” = first, “gynous”, as in gynecology = female). Among coral reef fishes, protogynous hermaphrodites are far more common than protandrous hermaphrodites.

In Curacao, and throughout the Caribbean, one species of protogynous hermaphrodite is especially common, called the yellowhead wrasse (Halichoeres garnoti). All yellowhead wrasses begin life with gonads that have not yet matured into either ovaries or testes but have more characteristics of an ovary. This is called the juvenile stage. Here’s a photo of a juvenile yellowhead wrasse: (https://reefguide.org/pixhtml/yellowheadwrasse17.html). If an individual is one of the fortunate few to survive the juvenile stage, it will mature into an adult female, pictured here (https://reefguide.org/pixhtml/yellowheadwrasse15.html). This is called the initial phase. It will then go through at least one reproductive season producing eggs. The larger females will then transform into males, the outward signs of which are obvious, as can be seen here: (https://reefguide.org/pixhtml/yellowheadwrasse18.html). Though less obvious, what occurs internally goes much deeper. The ovaries are transformed into testes. The large males are called the terminal phase, because it’s the end of the road of sexual differentiation in this species.

There are some interesting variations on the theme of protogynous hermaphroditism. Another common fish in Curacao is the bluehead wrasse (Thalassoma bifasciatum). It’s sexual development closely resembles that of the yellowhead wrasse: juvenile to initial phase to terminal phase males. But the initial phase of this species includes a small proportion of reproductive males. These initial phase males are outwardly identical to initial phase females, but with testes. Initial phase males, called primary males, don’t compete with the larger terminal phase (secondary) males for mates, which would be futile. No initial phase female would choose to mate with an initial phase male.

So initial phase males try to surreptitiously dump their sperm on a mating pair: initial phase female and terminal phase male. They are aided in this regard by their large testes, much larger in fact than those of the terminal phase males. These large testes allow for more indiscriminate release of large volumes of sperm. But the initial phase males must still obtain fairly close proximity to the mating pair if their sperm shower is to be effective. They are aided in this regard by their close resemblance to initial phase females. Even so, they must be hasty, because the terminal phase males are wary of this tactic and respond aggressively.

The six most common parrotfish species (family, Scaridae) in Curacao all share the reproductive life cycle of the bluehead wrasses: a few primary (initial phase) males and more secondary (terminal phase) males. But in all cases the terminal phase males far outnumber the initial phase males and enjoy more reproductive success. The three largest Caribbean parrotfishes have been completely fished out in Curacao. Of the remaining six, maximum size as been greatly reduced because the big boys are preferred by fishermen. In response to this source of mortality, females are transitioning to males at smaller sizes. I saw one terminal phase stoplight parrotfish (Sparisoma viride) that was only six inches, about a third the size of a typical terminal phase male in an undisturbed reef. It was similar but to a lesser extent for one of favorite parrotfishes in the Caribbean, the queen parrotfish (Scarus vetula). Here are images of the initial phase and terminal phase, respectively, of that species:

https://reefguide.org/pixhtml/queenparrot7.html; https://reefguide.org/pixhtml/queenparrot11.html

The ability of parrotfishes to adjust the timing of their sex change is a huge advantage in adapting to changing conditions. This sort of flexibility is called phenotypic plasticity, the capacity for developmental changes in a population that requires no genetic alterations. Sex change itself is a more fundamental form of phenotypic plasticity.

To this point, I have only scratched the surface of this form of phenotypic plasticity in teleost fishes. In the next post, I will consider the other form of sequential hermaphroditism, when males transform into females.