Jack-in-the-Pulpit Fishes
If the Male Thing Isn't Working Become a Female, or Vice Versa
In the previous installment of this series of posts, I discussed a remarkable plant called the Jack-in-the-pulpit which can change sex from year to year, depending on their energy stores. This degree of sexual flexibility is beyond the capacity of vertebrate animals, even fishes, the remarkable sexual lability of which I discussed in previous posts. At least that was the assumption until the 1990s. Turns out there are in fact fish species with Jack-in-the-pulpit-like flexibility, which can change from female to male and back in successive breeding seasons.
Many documented cases occur in one large family, the gobies (Gobiedae). Gobies, though common in many marine environments, are secretive, hiding in various orifices provided by coral, rocks, sponges, or burrows. As such, they tend to go unnoticed by snorkelers and Scuba divers alike. You must make a concerted effort to spot most goby species; even more effort—and patience—is required to observe their behavior in nature. It wasn’t until some goby species were maintained in captivity that their remarkable capacity for bidirectional sex change was first documented. Some of the sex switchers are monogamous, like clownfishes, some polygynous (one male, many females, i.e. haremic), like wrasses and parrotfishes, still other live in groups of multiple males and females.
Let’s first consider a monogamous species found in the tropical Indo-Pacific, one of the coral gobies (Paragobiodon), so called because they dwell in coral recesses. The redhead goby Paragobiodon echinocephalus, prefers a branching coral, Stylopholus. Those branches protect it from predators. Redhead gobies live in mated pairs, generally one pair per coral head.
Both male and female redheads can switch sex (https://doi.org/10.1093/beheco/5.4.434). So if one member of the pair, let’s say the male, should meet a bad end, one of two things can happen. The remaining female can pair up with another male that happens by. (She is reluctant to leave her coral shelter to search for a mate herself). Or, if it’s a lone female that happens by, she or the new arrival can transform into a male, usually the former. There is actually a third possibility. Any sexually immature individual in or around the coral head, can mature into whichever sex has gone missing, in this case a male. Jack-in-the-pulpits too can adjust their sex according to the number of males or females that live in the vicinity.
This sort of sexual flexibility is invaluable when your movement is restricted, either because, as in the Jack in the Pulpit, you are rooted in place; or, as in the case of the redhead goby, there are too many predators about to do much searching for a mate.
Another Jack-in-the-pulpit-like goby has completely different social arrangements. The orange-red pygmy goby, or Okinawa rubble goby (Trimma okinawae), is haremic, one male and several females dwell together in the interstices of coral rubble as the second common name suggests. The first common name indicates its color, which is prized by aquarists.
If the male rubble goby is removed, one of the females will become a male, as is the case for the protogynous species discussed in previous posts. But male rubble gobies can also become females under certain conditions. This is easiest to demonstrate in the lab, where the composition of groups can be manipulated. If a male is introduced into a harem with a bigger male already in residence, he will become a she ( https://doi.org/10.1111/j.1095-8649.2007.01338.x).
There is another goby variation on the Jack-in-the-pulpit theme, this one in a species that is the most familiar to me. It is a beautiful little fish—iridescent blue vertical stripes on a cardinal red background--quite common from California’s Channel Islands to Mexico’s Gulf of California. It is especially common around Catalina Island, which is the source of its alternate common name, the Catalina goby. It is more often recognized, common name-wise, as the blue-banded goby, by non-scientists, and Lythrypnus dalli, by scientists. I go back and forth, but I will call them blue-banded gobies henceforth.
Blue-banded gobies live in groups with several males and several females. Males are socially dominant, but some males are more socially dominant than others. Social status is directly correlated with male reproductive success. Since all females breed, males lower in the social hierarchy are more prone to switch to the female mode than those higher in the hierarchy. Conversely, higher ranking females are more prone to become males than lower ranking females. Each type of sex change occurs rapidly, a matter of days, especially in warmer waters (https://doi.org/10.1111/j.1095-8649.2007.01427.x).
Rapid sex change is characteristic of most bidirectional sex changers, but blue-banded gobies are exceptional because, like simultaneous hermaphrodites, their gonads have both ovarian and testicular regions, and they are capable of producing viable sperm and eggs. Unlike simultaneous hermaphrodites, though, they only produce one gamete type (sperm or egg) at a time. Hence, at any given time they are either functional males or functional females, not both.
In maintaining both functional ovaries and testes, the blue-banded gobies represent the apex of gonadal flexibility for a sex changing species. But all sex changing species, it turns out, maintain bipotential gonads. It’s just that the testicular tissue is regressed in females and the ovarian tissue regressed in males. The regressed tissue never completely disappears. An example of how this regressed tissue can be recommissioned occurs in the prototypical female to male sex changer, the cleaner wrasse (Labroides dimidiatus).
The common name, cleaner wrasse derives from the famous propensity of these relatively tiny fish to pick parasites off the scales and skin of much, much larger fishes, including potential predators such as groupers and snappers, often entering their open maws and exiting through the gills. They perform this service at specific prominent sites in the reef, called cleaning stations, at which their “clients” patiently wait their turn. There is no line cutting.
Like rubble gobies, cleaner wrasses are haremic, one male and several females occupy the cleaning station. The male is easily identified by his bright yellow coloration, in contrast to the blue and black lined females. When the male dies, or is removed in a field experiment, the largest female becomes a male, both internally (brain and gonad) and externally (coloration and behavior). The sex change in this species was among the first, if not the first to be documented, a paradigmatic case.
Recently, the cleaner wrasse story has developed a new twist, one that probably applies more broadly to sequential hermaphrodites. Tetsuo Kuwamura (https://doi.org/10.1046/j.1439-0310.2002.00791.x), who has studied these fish for decades, decided to try a simple experiment in a laboratory setting. He simply put to males together in the absence of any females. Surprisingly, rather than try to destroy each other—these are aggressive, highly territorial fish—one of the males, the smaller of the two, changed sex, that is, became a female. Subsequently, similarly reversed sex change has been observed in other protogynous species, including a wrasse (https://doi.org/10.1111/j.1095-8649.2007.01464.x ), a damselfish (10.1007/s10164-015-0450-8), an angelfish (https://doi.org/10.1007/s00114-011-0860-6), a hawkfish (https://doi.org/10.1111/j.1439-0310.2011.02005.x) and a grouper (https://doi.org/10.1046/j.1444-2906.2001.00287.x). These results suggest that the difference between those species labeled sequential hermaphrodites and those goby species called bidirectional sex changers is a matter of degree.
I find these sexually labile fishes fascinating in and of themselves. But what interests me more is what they tell us about some more general questions in evolutionary biology. Starting with, why, given the obvious advantages of sexual lability, haven’t more vertebrates evolved this capacity? We have a pretty good theory that explains when to change sex and which sex to change to, when sex change does occur. But this theory tells us nothing as to why sex change doesn’t occur in elephant seals, for example, or any other mammal, any other vertebrate (shark, amphibian, reptile or bird), for that matter. This is known as Williams’s paradox.