When the word hermaphrodite is uttered, it is often in hushed tones with references to grotesque, disparate rumors. In the world of biology, however, hermaphroditism is known to be a common and successful reproductive strategy among a wide variety of organisms. Plants, invertebrates, and many species of fish use hermaphroditism to ensure that their genes make it on to the next generation of individuals. This term in itself is not easily defined as there are many different forms; sequential, simultaneous, and self-fertilizing are a few of many broad classifications. In general, a hermaphrodite is an organism with both male and female sex organs during some stage in its life cycle. In order to fully understand hermaphroditism in fish and its evolutionary advantages, or lack thereof, we must look at the different forms and the varying ways that fishes use them. Hermaphroditism in fishes comes at a price for those that use it, but for many species it is the only way to ensure survival in a harsh world.
A fantastical depiction of a hermaphrodite in Le Louvre. (Photo by Paul H.)
Most common in fishes is sequential hermaphroditism, meaning that the fish starts life as one gender and at some point, due to genetic or environmental factors, morphs into the opposite sex. The process of changing sex from female to male is called protogyny, and this is the most widely used form of sequential hermaphroditism (75%). The other form, switching from male to female, is termed protandry (25%). Groupers (Serranidae), porgies (Sparidae), wrasses (Labridae), parrotfishes (Scaridae), angelfishes (Pomacanthidae), and gobies (Gobiidae) are all fish that are protogynous. For example, moon wrasse populations are made up of drab females, drab primary males, and gaudy secondary protogynous males. A secondary male, which began life as a female, may control a harem of females and mate with them individually while the primary males, each born with a single set of male reproductive organs, must aggregate in large groups to spawn with a single female (Robertson and Choat 1974). Examples of protandrous fishes are damselfishes (Pomacentridae). Several species of clownfish live in small hierarchical groups in a single anemone. There is a dominant female, a smaller mating male, and several non-reproducing males with no functional gonads. Only when one of the mating pair dies does the next highest ranking male step up and take on the sexual transformation (Fricke and Fricke 1977). Sequential hermaphroditism is an advantage for many fishes because it allows them to overcome the challenges of population structure biases.
Simultaneous hermaphroditism is exactly as it sounds: the fish has both male and female gonads at the same time. While this is relatively uncommon in fishes, there are several species that exhibit this characteristic in the family Serranidae. These fish may take turns fulfilling each role over the course of multiple mating events. For these groups of fishes, this life history could be the only way to ensure the survival of a population. Simultaneous hermaphroditism is an incredibly valuable trait when mating opportunities are rare due to sparse or dispersed individuals—it ensures that when two fish do cross paths, they are always compatible. It also balances the cost of paternal and maternal energy allocation when resources are in short supply. These fish can be said to be the ultimate compromisers and opportunists. While there are obvious benefits for some species of fish in extreme situations, simultaneous hermaphroditism can be difficult to develop because individuals must evolve congruent yet identical genitalia (Michiels 1998).
|Internal anatomy of a simultaneously hermaphroditic salmon. (Image from http://www.piscatorialpursuits.com|
It is rare to find a fish in nature that is a self-fertilizing simultaneous hermaphrodite. When an organism uses its own sperm to fertilize its own eggs, this process is called selfing and results in genetically identical offspring, also known as clones. Far from science fiction, this act insures that an individual’s genes are passed on regardless of circumstance. The Mangrove Killifish, for example, is a self-fertilizing hermaphrodite, but there are still some male-only fish in the population. While the mangrove killifish are able to survive and reproduce on their own no matter the conditions, it is the breeding with the males that introduces genetic diversity and ensure the survival and adaptability of the population as a whole (Grageda, et al. 2005). Without this outcrossing of genes, the Mangrove Killifish would vulnerable to extinction due to a very small gene pool. As we can see here, cloning is a useful strategy in situations where fish are far and few between, but it isn’t a proper substitute for traditional breeding practices.
In conclusion, hermaphroditism in its many forms is a unique adaptation evolved over the course of history to increase the survivorship of the species that use these methods. In populations of fish where individuals are less likely to come in contact with one another, simultaneous hermaphroditism raises the probability of an encounter with another fish being breeding compatible from 50% all the way to 100%. In sequential species, hermaphroditism plays a crucial role in behavioral rituals and sex ratios. Most oddly of all, self-fertilizing hermaphrodites are able to create a prodigy of their own even if they never come in contact with another of their species throughout their entire lives. Many of these strategies come with trade-offs of their own, especially the genetic issues with selfing hermaphroditism, but in the end it is better to have a compromised existence than none at all. Natural selection has given these species of fish what they need to endure in even the most desperate of circumstances.
Fricke, H., and S. Fricke. 1977. Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266:830-832.
Grageda, V. C., et al. 2005. Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus. Environmental Biology of Fishes 73:427-436.
Michiels, N. C. 1998. Mating conflicts and sperm competition in simultaneous hermaphrodites. Pages 219-254 in T. R. Birkhead and A. P. Moller, editors. Sperm competition and sexual selection. Academic Press, San Diego, California.
Robertson, D. R., and J. H. Choat. 1974. Protogynous hermaphroditism and social systems in labrid fish. Proceedings of the Second International Coral Reef Symposium 1:217-225.