Male or Female?
It Depends on When You Ask

‘Finding Nemo’, the highly successful computer-animated film by Pixar Animation Studios and Walt Disney Pictures, opens with a tragedy. A pair of Clownfish (Anemonefish, or Amphiprioninae) enjoy their new home and the eggs they have laid, when a large fish arrives and devours the female and most of the eggs, leaving only one to the widowed father. 

This story is indeed heartbreaking, but the filmmakers have omitted (or most likely, deliberately decided not to include) one of the potentially strangest features of such a situation. In the film, the disaster causes Marlin, the father, to turn from an adventurous fish into a worried and overprotective father. Had such a situation occurred with real Clownfish in nature, Marlin would have undergone a much more dramatic transformation: he would have become a female.

The opening scene from ‘Finding Nemo’:

Both male and female, but not always simultaneously

A spontaneous sex change, from male to female or from female to male, seems very strange to us, but is in fact quite common in many groups of animals. Nearly 5-6 percent of all animal species are hermaphrodites, producing both egg and sperm cells. Some, like snails, are simultaneous hermaphrodites: they have both male and female reproductive organs, both ovaries and testicles, simultaneously. Others can produce only one type of gametes at any given time, eggs or sperm, but are able to switch to produce the other type. These are the sequential hermaphrodites, who begin their lives as males and become females, or vice versa, and in some species this transformation can even occur several times during the life of the organism. 

Sequential hermaphrodites can be found in all animal phyla - Porifera, Cnidaria, Annelida, Mollusca, Arthropoda, as well as Vertebrata, the phylum we belong to. However, among vertebrates, gender switch is known only for fish, likely explaining why it is that we find this phenomenon so strange and unusual. The animals we share our lives with - those we are most familiar with -  tend to be either mammals, birds or reptiles - none of whom change their sex spontaneously.

The advantage of size

Why would a living organism change its birth sex? For a male, becoming a female would require the development of a tissue able to produce eggs, which are profoundly different from sperm, while in certain species this would also imply a change in body structure, color, behaviour and more. These are complex and energetically costly changes, and such an ability does not usually develop throughout evolution unless it provides the organism with a certain advantage.

Begin their lives as females and can become males when they grow large enough. Klunzinger's wrasse | Image: Elena Podolnaya, Shutterstock

Most studies that have examined sex changes focused on various species of fish, and therefore most of the existing information regarding possible causes  for the phenomenon comes from these animals. These studies show that for most gender-switching fish species, the key to the development of this ability throughout evolution lies in their size. A sex change usually occurs in a species in which size is highly important for the reproductive success of one gender, be it the male or the female, but relatively regligible for that of its counterpart. When a large male produces many more offspring compared to a small one, whereas the reproductive success of the female is not really size dependent, the best strategy for such fish would be to begin their lives as females, followed by a later transformation into males. The opposite is true for species in which the number of offspring the female produces depends on her size, rather than on the size of the male. 

In which situation does a male’s reproductive success depend on its size? This is relevant when the social structure of a fish species is polygamous, implying that they live in groups consisting of a single male and several females. The males then compete for access to the females, and thus for the right to reproduce: a weak male that controls a group of females is bound to be defeated by an ambitious stronger male. The larger fish are also the strongest, having a higher chance to defeat the other males. It is therefore beneficial for such fish to begin their lives as females, and to change their gender only after having grown big enough to successfully compete with other males - a phenomenon known-as Protogyny. 

This is the case, for example, with the Labridae, reef fish, many of which are decorated with bright colors. Several of these species, such as Klunzinger's wrasse (Thalassoma rueppellii) and the Clown coris (Coris aygula) can be found in the Gulf of Eilat on the Red Sea. The most extensively researched species in this family is the Blueheaded Wrasse (Thalassoma bifasciatum), who lives in the Caribbean Sea. The males of this species are highly territorial, maintaining a habitat in which multiple females live and lay eggs. Interestingly, when a male that dominates over such a territory dies, the largest female in the habitat will usually become a male, “inheriting” the territory. As part of the process the former-female not only begins to produce sperm but also changes her color and behaviour. These changes can occur very quickly: when researchers distanced the males from a population of Wrasse, the larger females - who had laid eggs only one day earlier - began acting as males in a matter of minutes, releasing sperm that same day.

Large females can produce more eggs. A Maroon Clownfish female (right) and male (Spine-cheeked Anemonefish) | Image: Bernard Dupont, flickr

From a small male to a large female

The opposite sex switch is common in fish species that form monogamous couples, or in those that breed more or less randomly. The fish begin their lives as males and later become females, a phenomenon known as Protandry (“male-first”). The sex change provides them with an advantage, not due to competition between the females and the males, but because the number of eggs they are able to produce is directly related to their size. Sperm cells are small and relatively “cheap” to produce in terms of the resources the male has to invest in them, whereas eggs are much larger and require a more significant investment. Not only is the egg cell itself larger than the sperm, but fish eggs, similar to the eggs of other species, contain nutrients required for the fetus during its development. Larger female fish are capable of producing and storing more eggs in their abdomen, and will therefore have an advantage over smaller females. 

An example of that are the Anemonefish, like Nemo and his father. Anemonefish usually live in small groups consisting of an alpha couple - a specific male and female who are the only ones to reproduce - and a few younger fish. In the case that the female dies, the alpha male becomes a female and the largest of the younger fish who reaches sexual maturity takes the place of the former male in the pair. In the movie “Finding Nemo'' Nemo and his father live together, with no other Anemonefish. Had father Marlin become a female, following the events that open the story, this would likely have driven Nemo to reach sexual maturity and then… Probably best not to think about it.   

Why is it that the young male fish do not reproduce? At first glance it would  seem that had they been females who mate with the alpha male, similar to the situation in Labridae, Anemonefish would have gained greater reproductive success. The answer, as it seems, lies in the limited space available to them. Anemonefish live in mutualistic symbiosis with the Sea anemones, whose stinging tentacles do not harm them, but protect them from predators. Anemonefish gain from this “deal”, but this means that the space available to them to lay eggs and live in, is limited by the supply of sea anemones in the area. A model that was developed by a researcher from Japan demonstrated that under these conditions, a monogamous lifestyle, similar to the one seemingly present in Anemonefish, will allow for more offspring.

Goby fish change their gender back and forth routinely, not only under specific conditions. Citrinis (right) and Emerald coral goby (left) | Image: Madelein Wolfaardt (right), Mike Workman (left), Shutterstock

Female - male - female

The third group of sequential hermaphrodites contains those species that have a hard time deciding: they can switch from female to male and also from male to female, and sometimes undergo this change more than once. In some cases these are protogynous fish, which normally switch from females to males, but under certain conditions they can also switch back to become females. An example for that is the Bluestreak cleaner wrasse (Labroides dimidiatus), a fish of the Labridae family, that can be found in the Gulf of Eilat. When researchers distanced the females of a population of wrasses in a reef near the coast of Japan, some of the widowed males, who were left without a mate, moved to new territories, joined the flock as mates to a male. The smaller and weaker male of the pair switched back into a female. 

Some fish change their gender back and forth routinely and not only under such special conditions. Such are the reef dwelling Goby fish (Gobiidae) Paragobiodon and Gobiodon, among others. These fish live between the “branches” of corals such as the Acropora, where they are relatively protected  from predators. In order to find mates many of them have to leave their coral colony and visit a nearby colony, a journey that involves a great deal of risk. Researchers speculate that their ability to change their gender in both directions - male to female and female to male - has evolved in order to reduce the dangerous journeys they are forced to undertake. When a male Goby fish reaches a coral with a male but no females, there is no need for him to continue his journey to a different coral: one of the males simply becomes a female, which enables them to reproduce. The same is true for the case when a female Goby fish arrives at a coral to find a female-only population. 

How do they decide which of the two will switch gender? In Goby fish, size confers an advantage to both males and females, but females grow faster than males. It therefore makes more sense for the smaller fish to be female and thus to “catch up” on its counterpart in terms of size. Studies have demonstrated that indeed, when such a couple starts off as two males, the smaller male will turn into a female, whereas when they begin as two females, the larger female will become a male. However, when the couple originally meets as a male and a female, they remain in their original gender - even if the female is larger than the male.  Although there appears to be an advantage for the smaller fish to be female, it is not large enough to justify the investment of resources required for a sex change, when one is not absolutely necessary.

Some of the Thalassoma develop originally as males, but disguise as females. A male Blueheaded Wrasse near some females or perhaps initial-phase male yellow fish | Image: Rob Atherton, Shutterstock

A male in female skin

Finally, just to complicate the picture even further, some fish seem dissatisfied with the method utilized by their species and choose a different path. Remember the Blueheaded Wrasse, of the Labridae family? Most wrasses begin their lives as females, turning later into males that dominate a territory in which females lay their eggs. Not all behave similarly, however. A small portion of wrasses skip the female phase entirely, developing originally as males. These males are very different from the large, territorial males, who were once females: these male wrasses, termed Initial-phase males (IP males), are small, their colors are fainter, and they highly resemble females.   

Their size does not allow them to compete with the larger colorful males, nor do they try to. The IP males have no territory of their own, and they reproduce in a manner that might not seem particularly decent: when a female lays her eggs in the territory of one of the large males, the small IP male sneaks in and fertilizes a some of them, before the large male has had a chance to do so. His female-like appearance apparently allows him to roam the territory of the large male without being attacked by him. 

Studies have demonstrated that IP males appear mainly in crowded populations of wrasses, in which the competition for territory between males  is particularly fierce. They represent another strategy by which the fish succeed in passing on their genes to the next generation, this time not by switching their sex, but by pretending to belong to the opposite one.