In the first episode of Blue Planet II we met the Kobudai – the Asian sheepshead wrasse - that was introduced as a female, behaved like a female and looked like a female. And then, as we watched she slowly but surely morphed into a male – displayed male behaviours and developed male characteristics. It may seem strange but in fact it's common among fish. Known as sequential hermaphrodism, sex change is a common and usual adaptive part of the life cycle. It is documented in at least 27 families of fish, spread across nine orders and displays three patterns: changing from female to male, known as protogyny; changing from male to female, known as protandry; and serial bidirectional sex change. All three types of sex change occurs across the teleost tree of life, which suggest that it has evolved multiple times – but why?
The biological processes and adaptive advantages of sex change has fascinated scientists for decades and the ecological and evolutionary contexts in which it occurs is now quite well studied and understood. The dominant theory as to why it occurs is known as the size advantage model. According to this model, changing sex is adaptive if your reproductive value (the number of offspring you can produce) is greater when you are a female when small, but a male when you are older and hence larger (as in the Kobudai) or vice versa. So by changing sex, lifetime reproductive success is maximized (the combined number of offspring you produce as a female and then a male or the other way round). Whether or not a species in protandrous or protogynous depends on their mating system and social structure. Protogyny – changing from a female to a male – is more common in fish than protandry because many fish have a mating system where large males, because of their superior competitive ability (in fights and contests with smaller males), are able to monopolize females and prevent smaller males from mating with them. Under these circumstances, reproducing initially as a female when small and then changing sex and becoming a male when large is the best strategy in order to maximize the number of offspring you leave in the next generation.
Female to male change is common in the social wrasses like the blue headed wrasse and the Kobedai (though little is known about this species). The mating system is such that, large dominant males defend spawning sites which females need to lay their eggs so only males that are big enough to defend these sites are likely to mate. The best option her then, is to be a female when you are small and once you grow large enough, change into a male. In the blue headed wrasse, loss of the dominant male stimulates sex change in the largest female (typically) of the social group and involves dramatic changes in behaviour, anatomy and colouration.
Most juvenile blue headed wrasses develop as females but a few develop into small female-mimic males. These males are known as sneaker males, which try and sneak matings with females without the dominant male realizing. The number of fish that develop into sneaker males is also dependent on the social structure of the group – more sneaker males occur in groups where the density of fish is high and the ability of dominant males to monopolize females is reduced. A recent study suggests that in the Kobudai there are no sneaker males – males are derived directly from females.
In species that change from male to female, the mating system in different usually consisting of monogamous pairs (where males and females pair during the breeding season and stay together and the male usually helps in looking after eggs) or where mating is random with respect to size. So, in these species male size doesn’t influence whether or not you mate with a female. But, larger females produce many more eggs than small females so it is adaptive to change to a female when large. For example, some species of anemone fish (one of which you will meet in the episode “Coasts”) live in small groups consisting of a small male and a dominant female plus smaller subordinate non-breeding individuals. The loss of the dominant female prompts the male to change sex and become the dominant female and one of the immature fish to become the new breeding male.
Fish that change back and forth between sexes is much rarer but is the strategy adopted by some species of coral gobi. It is not easily explained by the size advantage model however. Current thinking is that coral gobis experience limited mating opportunities because they live in specialized niches and seldom move between isolated colonies of coral due to predation risk. The ability to change sex in either direction makes it easier for any two fish to form a pair without moving and also reduces the time between breeding events.
How does sex change occur?
In many sequential hermaphrodite fishes, tissues of both sexes are present in the gonad prior to sex change whereas in others reproductive tissues are completely replaced by the secondary sex. In wrasses, complete restructuring of reproductive tissues occurs because no testicular tissue is present in the ovary prior to sex change. This transformation can occur rapidly, in the blue-headed wrasse taking as little as 8 days. Sexual differentiation and gonadal development in fish depends on the balance between oestrogen (female hormone) and androgen (male hormone) production. In sex changing fishes, dramatic shifts in sex hormones accompany gonadal sex change but what tips the balance towards male or female steroid production remains unclear.
If you would like to learn more about the adaptive reproductive strategies employed by animals to maximize mating success as well as the evolutionary implications you may consider studying S295 The biology of survival and S317 Biological Science: from genes to species.