Week 06: Sequential Hermaphroditism (or why to be wary of frog DNA)

Last week, we discussed one type of hermaphroditism: simultaneous (also known as synchronous) hermaphroditism, in which an individual produces both eggs and sperm at the same time (see Serena’s awesome blog post here for more info!)

This week, we moved on to the other type of hermaphroditism: sequential hermaphroditism. A sequential hermaphrodite is an individual that changes (or has the capability to change) sex at some point in its life, meaning it can produce both eggs and sperm over the course of its lifetime (but not at the same time). A sequential hermaphrodite can start as female and change to male (called protogyny, meaning “female first”) or start as male and change to female (called protandry, meaning “male first”).

Sequential hermaphroditism is widespread among plants, invertebrates (including some snails, sea stars, etc.), and fish. I didn’t know it at the time, but I was first introduced to the idea of sequential hermaphrodites in one of my favorite movies: Jurassic Park. In case you have never watched Jurassic Park (blasphemy!) or have forgotten the details, the lead scientist is sure that the dinosaurs they have created are unable to reproduce because they were designed to all be female. However, as Jeff Goldblum’s character famously points out:

In the film, some of the female dinosaurs change into males and successfully produce offspring because the scientists used frog DNA to fill in gaps in the dinosaur DNA. While Jurassic Park is a blend of scientific reality and imagination, some frogs really can change from female to male (and are thus an example of protogyny in real life).

Another sequential hermaphrodite that has caught the public’s attention in recent years is the clownfish of Finding Nemo fame.

Picture1.png

modified from SMBC comics

As described in more detail on a post from The Fisheries Blog called “Finding Nemo lied to you” (check it out here). In the movie, Nemo’s mother gets eaten by a barracuda, so Nemo grows up under the watchful eye of his father before getting lost and causing his father to go on a wacky adventure to get Nemo back. If Finding Nemo were biologically accurate, Nemo’s father would have changed into a female after the death of Nemo’s mother and Nemo would have become his father’s mate. While this would not necessarily make a great light-hearted Disney film, it does provide an example of a species that can change between sexes based on the social situation.

So why are some species sequentially hermaphroditic? One of the earliest explanations is the size advantage hypothesis, which suggests that sequential hermaphroditism can be advantageous if an individual that spends part of its life as a male and part of its life as a female has a higher overall (lifetime) reproductive potential compared to an individual that stays the same sex. Since a male can produce many sperm with little investment per gamete but a female generally invests more resources into producing each egg, female reproductive potential can increase with age as the female grows larger and thus has more resources to invest in egg production. If mating is random, this situation would favor changing from male to female.

Picture2.png

Random mating and female reproductive potential increasing with age is hypothesized to favor a change from male to female (modified from Warner 1975)

On the other hand, if mating is not random and male reproductive potential increases with age or size, this would favor changing from female to male. For example, male inexperience, territoriality and dominance by older males, or female preference for larger males would tend to produce this result.

Picture3.png

Non-random mating is hypothesized to favor a change from female to male (modified from Warner 1975)

Since its creation, the size advantage hypothesis has been expanded into the expected reproductive success threshold (ERST model) to also include size-fecundity skew and sperm competition (defined below). The idea here is that even if the above situation seems to hold, the largest females do not always change into males when the opportunity arises. In this case, the ERST model suggests that size-fecundity skew and/or sperm competition explain this phenomenon.

Size-fecundity skew means that the fecundity (expected reproductive success) of a female can be so high that changing to a male would not increase her expected reproductive success. In harem situations, this can occur because a female is so large that her fecundity is higher than the combined fecundities of all the other females; even if the large female changed to a male and mated with all other females in the group, this would not increase the expected reproductive success. This hypothesis is supported by cases in which a smaller female will change to a male when the male is removed from the group.

Similarly, sperm competition due to the presence of multiple breeding males (paternity dilution) would also lower the expected male reproductive success. This could also cause smaller females to undergo sex change instead of the largest females.

Finally, a really cool paper by Sakai et al. (2003) shows how fish can not only change sex (whether the individual produces sperm or eggs) but also change gender (appearance, behavior, and life history) and reverse those changes. Centropyge ferrugata angelfish all begin as females, but some individuals become males and maintain harems of females. The males have different coloring and behavior compared to females, but in experimental pairs of two males, often the smaller male would reverse its coloring to that of a female and perform female mating behavior in addition to producing eggs.

Overall, this week was an interesting topic that showed that sex and gender are often not as fixed as we might think.

-Lauren

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modified from The Insightful Panda

Resources

Warner, R. R. (1975). The adaptive significance of sequential hermaphroditism in animals. American Naturalist, 61-82. PDF

Muñoz, R. C., & Warner, R. R. (2004). Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians. Behavioral Ecology15(1), 129-136. PDF

Sakai, Y., Karino, K., Kuwamura, T., Nakashima, Y., & Maruo, Y. (2003). Sexually dichromatic protogynous angelfish Centropyge ferrugata (Pomacanthidae) males can change back to females. Zoological science20(5), 627-633. PDF

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