Hermaphroditism under the sea – a whole different kettle of fish

Were you left with a bittersweet taste in your mouth as the credits of Disney Pixar’s “Finding Nemo” began to roll? Yes – it was all very happy and uplifting when Nemo was found in P. Sherman’s dentist’s surgery on 42 Wallaby Way, after a hugely treacherous yet highly entertaining adventure across the indo-pacific ocean. But, the sad truth of the matter is that Nemo returned to his anemone home as a motherless child…or did he? What you may not know about clownfish is that they are experts in the art of sex change and that by the time Nemo had returned to the family fold his father, Marlin, would have in fact transformed into his mother – Marlina if you will.

Sex change and hermaphroditism are common to many different families of fish. Sex change can be male to female (successive protandrous), female to male (successive protogynous), or from neutral juveniles into either of the sexes (gonochronistic). Some fish will never actually change sex and retain both male and female genitalia throughout their lifetime (synchronous hermaphroditism). The more socially conservative amongst you might now be asking why such an apparently perverse behavioural trait would have possibly evolved?

It was originally thought that synchronous hermaphroditism evolved in solitary species that live in the open ocean (such as white bass) in order to be able to self-fertilise in an environment where individuals very rarely come across a potential mate. However, exclusive self-fertilisation would lead to dramatic inbreeding and the rapid extinction of the species. It is now thought that synchronous hermaphroditism probably evolved to ensure mating success when solitary roamers do happen across each other. If we imagine for a minute that the white bass was constrained by social convention and that the population had a constant sex ratio of 50:50. This would mean that 50% of the time that one individual comes across another of the same species they will be interacting with an individual of the same sex as themselves. By retaining both male and female genitalia they ensure that they can mate with whoever it is that they come across – this is a way of ensuring successful reproduction in a low density population without incurring the wrath of inbreeding!

In gonochronistic hermaphroditism all juveniles are neutral but as they develop into adulthood they lose one set of genitalia and retain the other in order to develop a discrete sex. If a juvenile finds itself in a particularly female-dominated population then it will lose its’ ovaries and retain its’ testes in order to become fully male thus reducing mate competition and increasing the number of offspring they will pass into the next generation. This is all well and good but why is sex not allocated in the egg according to the current sex ratio of the parental population? Juveniles are unable to reproduce so they have no need to have a discrete sex. By being indecisive and non-committal at an early stage the individual is therefore taking the most advantageous decision that will allow them to maximise their reproductive output at the point of mating.

The main hypothesised advantage associated with protandrous successive hermaphroditism (male to female sex change) is the “size-advantage model” and this is perfectly exemplified by the clownfish. Females are more fertile when they are larger simply because eggs are large cells that are metabolically expensive to produce and therefore require a large home in which to be created and stored. Sperm is small and cheap to produce so that smaller individuals are reproductively successful as males – there are some species where small males are up to 100 times more fertile than females of the same size! By changing sex throughout their lifetime fish are, again, able to maximise the number of offspring that they have in the next generation.

Female to male sex change (successive protogynous hermaphroditism) is perhaps the most important of these sexual phenomena for us to understand in terms of our approach towards fisheries management. Protogynous fish live in large harems where the dominant male has the mating rights to all females within the group and the subordinate males are generally reproductively redundant. Protogynous species display a large amount of sexual dimorphism – females and secondary males tend to be much smaller with very dull colouration whereas males are large and brightly coloured. At first this seems like it might be disadvantageous to the dominant male – bright colours are metabolically expensive to produce and whilst they facilitate mate finding they make you more conspicuous to predation. However, the pros seem to outweigh the cons as the increased risk of predation is offset by the increased reproductive success.

So how does sex change actually occur? In female to male sex change the process occurs as a result of hormonal changes that are stimulated in females by certain social cues. If the dominant male is removed from the group, the dominant female will begin to display more aggressive behaviour – she is now known as a “behavioural male”. Her behaviour will trigger the release of testosterone and will inhibit the production of enzymes that breakdown “male” hormones in the brain (aromatases) – this will increase the aggressiveness of the “behavioural male”. In turn this will lead to the production of testosterone in the reduced testes of the dominant female which then causes the morphological shift from female to male as the testes become larger and the ovaries disappear – changes in colouration occur in conjunction with the changes in genital organisation.

However, there are exceptions to the above rule and under some circumstances it is possible for there to be more than one male in a harem. In overcrowded conditions you will often find that there are multiple males. Females are able to gauge the number of male and female interactions that they have in a given period of time. If the dominant female has too few a number of interactions with males then she will detect a gap in the reproductive market and transform into a male herself. The transformation of multiple subordinate females into primary males is facilitated by the overcrowded conditions themselves. Subordinate females which would not be able to transform under normal circumstances, as a result of naturally low testosterone levels, find themselves becoming male. Their testosterone levels are increased artificially as a result of higher levels of the hormone being present in the water due to the large number of fish living in their direct environment when conditions are overcrowded.

Understanding the intricacies of sex change in fish could prove to be vital in altering our approaches to fisheries management. Groupers are a very good example of commercially important protogynous fish that must be small females before they are able to develop into large males. If we are removing groupers from the ocean before they have had an opportunity to become male then we are effectively condemning their populations to extinction. By understanding sex change we can place restraints on sizes of fish that are allowed to be caught and hopefully go some way to replenishing our ocean’s stocks.