On with the show:
The array of animals that maintain sex organs for producing eggs (female sex cells) and sperm (male sex cells), called hermaphrodites, is vast. You can find one if you grab a net and spend about 15 minutes at your local pond. While some animals are both sexes at the same time (simultaneous hermaphrodites), others change sex over their lifespan (sequential hermaphrodites). I spend a lot of time with simultaneous hermaphrodites (freshwater snails), so I was interested in finding out more about the incidence of sequential hermaphrodites.
If you change sex, which sex do you start with? Usually, biologist tag being male as less energetically expensive; sperm are cheap to make, so it might make sense to begin as a male, and then when you get larger with more energy reserves, you swap to female. This style is called protandry. And although it seems the most practical energy use wise, the other mode, protogyny (female first), is also observed. Is the male first more common? Can some animals change and then change back? What other mysteries await?
Sequential hermaphroditism is observed among snails, crustaceans, and fish. I took a deeper dive into the fish because fish are fascinating.
An Aside:
FYI, I know that fish are not supposed to exist anymore; that is the mono-phylogenetic group called fish. However, we can defend fish by using that term just for the ray-finned fishes of the world. Thus, sharks are no longer considered fish. The Coelacanth, not a fish. Lungfish, no longer a fish. Whoa, wait, I was getting distracted; this will be another blog. Back to sex and fish, that is, ray-finned fishes.
Another Aside:
I have ranted on the overuse of terminology, something biology has in spades, so it will come as no surprise that I am not a fan of the terms protogyny and protandry. Male-first or female-first flows so much better. Alas, here we are in this current world.
First, the fact that surprised me, protogyny, which is female-first, is common among the fishes that change sex. This is found in fish that guard or otherwise aggressively control/protect a territory or a cluster of fish (young and female). Being a large male is beneficial in this situation, common among wrasses, Family Labridae.
The bluehead wrasse, Thalassoma bifasciatum, found in the Caribbean. By the way, I’m resisting a rant on this poorly-named fish. Poorly named because the bluehead is only observed in the terminal phase of males. These fish can be born male or female, but if born female can change sex from female to male. The females and smaller males do not have the distinct blue head.
FYI, the dreaded terminology/ acronym brew-ha-ha that is science. In a group of wrasses, the large blue-headed male is in what is known as Terminal Phase (TP). Large females (with different coloration) are in what is known as the Initial Phase (IP).
Parrotfishes:
Parrotfishes and wrasses are now considered in the same family, Labridae. Historically Parrotfishes were in their own family, Scaridae.
Parrotfishes are one of the most studied in the realm of sex change. Similar to their relatives, the bluehead wrasse, females can change to become males, with the males playing the protective/dominating role among a hoard of females and youngsters.
Identifying these species on the reef can be challenging because of the color changes. Similar to the wrasses, the big males are in Terminal Phase (TP), females (with different coloration) are in the Initial Phase (IP), and juveniles look different than the others having different background color and white spots. Sometimes females can become males but do not change color or do not change color immediately. These are called Initial Phase Males. We might call this cross-dressing.
Yes.
The famed Finding Nemo fish, clownfish, start as males and swap to females.
At least 500 other fish species can (or do) change sex, with at least one species, the Australian Blue-banded Goby (Lythrypnus dalli), being able to change sex and then change back. All juveniles initially become female; later, some change to male. The male can change back to female, but these later ‘changers’ are true hermaphrodites containing eggs and sperm.
Full circle back to the simultaneous hermaphrodites:
Some kind of sex change, including true (simultaneous) hermaphroditism, is not uncommon in fishes; found in more than 450 species in 41 families. True hermaphrodites are found in 13 families. Sex-changing is found in marine and freshwater fishes but appears more common in marine fishes.
There are still many unknowns; the mating systems, and behaviors et al., are known from about 60% of the sex-changing fishes: Much more to discover out there.
Sources and Further Reading:
Barlow G. 2000. The Cichlid Fishes: Nature’s Grand Experiment in Evolution. Perseus
Cardwell JR, Liley NR. Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. 1991. Gen Comp Endocrinol 81(1): 7-20. doi: 10.1016/0016-6480(91)90120-u. PMID: 2026318.
A bioRx Pre-print:
Goikoetxea A, Muncaster S, Todd EV, Lokman PM, Robertson HA, De Farias e Moraes CE, Damsteeg EL, and Gemmell NJ. 2021. Sex change in aquarium systems establishes the New Zealand spotty wrasse (Notolabrus celidotus) as a temperate model species for the investigation of sequential hermaphroditism.bioRxiv preprint: https://doi.org/10.1101/2020.08.28.271973
Hodge, J.R., Santini, F. and Wainwright, P.C., 2020. Correlated evolution of sex allocation and mating system in wrasses and parrotfishes. The American Naturalist 196(1): 57-73.
Kuwamura T, Sunobe T, Sakai Y, Kadota T, and Sawada K. 2020. Hermaphroditism in fishes: an annotated list of species, phylogeny, and mating system. Ichthyological Research 67:341–360.
Roughgarden, J. 2013. Evolution’s Rainbow: Diversity, Gender, and Sexuality in Nature and People. University of California Press, Berkeley. pp. 137-38.
Warner RR, Swearer SE. 1991. Social Control of Sex Change in the Bluehead Wrasse, Thalassoma bifasciatum (Pisces: Labridae). Biological Bulletin 181(2):199-204. doi: 10.2307/1542090. PMID: 29304633.