Is there anything fish don't do!? Mucus-feeding and prolactin

Much of my work involves studying fish genomes. Over time I've gotten to know them pretty well and I can only conclude that fish are incredible and inordinately interesting creatures. Unfortunately fish have an undeservedly low standing in the eyes of the general public, as well as many researchers in more mammal-oriented fields, often being referred to as "lower vertebrates" in the great evolutionary story that led to "higher vertebrates" like mammals. In fact, more than half of all vertebrate species are fish, not "higher vertebrates", and fish encompass the great majority of all vertebrate diversity. In most senses fish are the "typical" vertebrates. Their origin set the whole stage for vertebrate development, anatomy and physiology and the fair view of vertebrate evolution should be that reptiles, birds and mammals, basically everything that lives on land, are a subgroup of highly specialized fish, an interesting "side-step" rather than the "crown" of evolution.

So why this preface in defense of fish? I have found a little story that more than anything I've read lately highlights the deep connection between fish and mammals and does a very good job at blurring the distinction between what's considered typically mammal and what fish are capable of. Plus, it relates to my own research.



Discus fish (Symphysodon aequifasciatus). Ref: Flickr.

Behold the discus fish.

The three discus fish species of the Amazon basin in the genus Symphysodon are something out of the ordinary in that they exhibit parental care behaviors and feed their fry with a special mucus secreted from both parents' skin. The fry start nibbling from the parents' skin a few days after hatching and continue for a up to 3 weeks before being "weaned off", in a phenomenon akin to mammal lactation. Not only does the composition of the mucus change as the fry grow in a way that mirrors the changes in the composition of milk in mammals, it also seems that there are shared mechanisms in the stimulation of discus fish mucus production and milk production in mammals. Discus fish are not the only fish species that have these qualities, but they have become the typical example, not least because they have been appreciated as aquarium fish for a long time. You can find and abundance of videos showing discus fish parental behaviors on YouTube.

The composition of non-parental skin mucus and parental skin mucus in discus fish is different. During breeding the mucus contains many antimicrobial proteins and factors that stimulate the regeneration of skin cells; this is to protect the parents from infections due to the fry's excessive nibbling. But the mucus also contains antibodies and factors that are thought to contribute to the fry's immunity during the very first period of life, akin to mammal milk. In another parallel, the levels of antibodies and proteins are at their peek around the time of hatching (birth) and decrease when it's time for "weaning".

In mammals the hormone prolactin, as the name indicates, regulates the production of milk through the prolactin receptors that are expressed on milk gland cells. However prolactin is a very old hormone (fish have prolactin too!) and probably the hormone that has the most known functions in all of endocrinology. In fish it mostly acts on the gills, the intestines and the kidneys to control the regulation of water balance in the body. This is probably one of the original roles of prolactin in the first vertebrates a few hundred million years ago. However, in both mammal and fish, including the discus fish, prolactin has been shown to stimulate parental care indicating that the effect on behavior also is old. Lactation on the other hand seems to be a relatively new function for prolactin and thus the name "promotor of lactation" is a misnomer if there ever was one. Or is it?


Ref: Khong et. al. (see reference below)

Studies of the expression of the prolactin receptor in the discus fish skin reveal that it's expressed in significantly increased numbers during the parental phase, as you can see in the figure above, indicating that it's prolactin that stimulates mucus production! What an incredible parallel! It's the closest thing to breast-feeding fish that you will ever find. The prolactin receptor also seems to mediate the creation of new mucous cells in the skin, further increasing mucus production and counteracting the effects of the fry's nibbling. The mucous cells of the skin are a kind of epithelial cells, so are the milk gland cells in mammals and the sweat gland cells that they share an origin with. So are the cells in the fish intestine and gills that are involved in water balance regulation. Do you see the pattern? Milk secretion, mucus secretion, sweating, the transport of water across a barrier are variants on the same theme.

The similarities between mammal lactation and discus fish parental mucus production could all be incidental, the result of convergent evolution, but the involvement of prolactin receptors in both processes speaks for there being a deep ancestral mechanism shared between lactation in mammals and mucus production in fish.

Buckley, J., Maunder, R., Foey, A., Pearce, J., Val, A., & Sloman, K. (2010). Biparental mucus feeding: a unique example of parental care in an Amazonian cichlid Journal of Experimental Biology, 213 (22), 3787-3795 DOI: 10.1242/jeb.042929

Khong, H., Kuah, M., Jaya-Ram, A., & Shu-Chien, A. (2009). Prolactin receptor mRNA is upregulated in discus fish (Symphysodon aequifasciata) skin during parental phase. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 153 (1), 18-28 DOI: 10.1016/j.cbpb.2009.01.005