The Dzwillo Base Body System in the Light of Current Cell Biology

Note: If you are looking for a critique of the Storozhev - Apryatin Base Body table (the so-called "Russian table") it is here.

The guppy "Base Body System" refers to a table that organizes guppy phenotypes into two basic categories, base body colors and secondary sex colors. It is widely used in Europe and to some extent in Asia to classify guppies into classes for judging at guppy shows. Although the current European base body system has expanded the list of base body colors, the basic theory of the Dzwillo system is unaltered.

Dzwillo's Two Layer Base Body System

The Base Body System traces back to a single scientific source, the paper by the German scientist Michael Dzwillo published in 1959 called, "Genetische Untersuchungen an domestizierten Stämmen von Lebistes reticulatus (PETERS)" Hamburg. Zool. Mus. Inst. I Band 57 1 S. 143-186 1 Hamburg, December 1959. The article roughly translates as "The Genetics of Domestic Strains of Lebistes reticulatus (PETERS)."

In the paper he begins by outlining what he calls the “base body” colors. What he is referring to is “background color."  Presumably this is the overall color of the guppy, minus the spots and other patterns seen as superimposed on the background. The latter are usually described as secondary sex colors, since they begin appearing as the guppy sexually matures. An example is the albino base body color. Under this system albino would be classified as a base body color and the half-black pattern (tuxedo in Asia) would be a secondary sex color. Albinos genetically remove black color, so an albino half-black guppy would lack the half-black pattern. If the guppy had red spots, the red color would be washed out without the base body black "behind" it.

Dzwillo notes that the base colors are present at birth and they are usually autosomal recessive.

Does the Base Body System actually have any basis in cell biology? If you search the scientific literature you will discover that the Base Body System has not been adopted as a model for the organization of colors and patterns in animals, certainly not in fish, and certainly not in guppies. You find the odd reference to foreground and background colors in animals, but nobody appears to have adopted it as a method of organizing color cells in fish, reptiles or amphibians. (Mammals have only one type of color cell, the melanocyte.)

Bagnara Introduces the Third Dimension

It is important to realize that Dzwillo published his paper in 1959. Just after he published his paper, in the early 1960s, the study of animal pigmentation went through rapid advancement. It is found in the work of Joseph Bagnara who studied the color patterns on non-mammalian animals. (He is author of non-mammalian chapter in the major tome on the pigmentary system called, "The Pigmentary System, Physiology and Pathophysiology" Oxford Press. You can actually read that chapter online at Google Books. Scroll back to page 10 or 11 for the beginning of the chapter.) In his work Bagnara paints a very different picture of the way that fish, amphibians and reptiles produce color and pattern. It is not a simple static two dimensional layering system. There is no simple background and foreground colors.

This diagram is an adaptation of one by Bagnara, showing the way the light is manipulated when it penetrates and is selectively reflected or refracted by the main color cell layers.

As you can see the color cells are organized into three layers. Black color cells at the bottom layer act to sponge up light that falls through the color cells. This prevents light from reflecting back through the skin to the eyes. The reason why albino guppies have pale reds, oranges or yellow color is that the absorbing level is missing, so the light is bouncing right back through the skin, washing out the red and yellow colors. (See path three in the diagram above for what happends to a light ray that passes through the layers of color cells and is absorbed by the black color cells or melanophores.)

The reflecting color cells (iridophores) bounce light back from the skin to the eye. The arrangement and pattern of the iridophores determines what color you see. Highly directional light will be seen as a silver color. Another arrangement of the purine platelets in the iridophores produces light our eyes detect as blue.

The top layer acts like color gels on theater lights...they selectively absorb all but red, yellow or orange (yellow plus red) light. Green color in the guppy is a combination of blue reflected light and yellow color cell filtering (blue plus yellow equals green).

The second path in the diagram above shows what happens when a mutation makes the iridophore level so dense that all the light is reflected before it even reaches the layer below. A separate mutation may make the red color cells dense. If the iridophores are arranged in such a way as to reflect intense (i.e. silver) light, we see red metallic color (red plus silver).

There is not a simple arrangement of a background color and foreground color, like two gels on a theater light. There is an interplay between three levels of color cells, each layer manipulating the light in very different ways. For example, the iridophore reflecting layer refracts light differently according to the spacing and arrangement of the reflecting platelets in the cell. It can produce the iridescent color you see around the gills of the guppy or the intense blue of the Japan Blue.

What is important about the Dzwillo paper is that it was the first paper in the guppy scientific literature that does take into account the layering of color cells. It was a step in the right direction. Before Dzwillo you do not find the guppy color system treated as layers. The color patterns described by Winge or Natali are entirely two dimensional. After Dzwillo you begin to see guppy color as dimensional.

Bagnara is responsible for another major insight into the development and expression of color cells. In a seminal paper written in 1979, "Common origin of pigment cells," Science Magazine, 2 February 1979, Bagnara et al., pp.410 - 415 (See Bagnara, http://www.sciencemag.org/cgi/content/abstract/203/4379/410) Bagnara proposes a kind of "stem" color cell from which all other color cells develop. To my mind this introduces the fourth dimension into the study of color cells in the guppy, time. You can actually see the late stages of this unfolding drama in the development of the secondary colors on male and female guppies. A particularly interesting example is the initial development of yellow color cells on guppies with the Magenta mutation. Around about three or four months these yellow color cells begin changing to red color cells. This change in colors can occur all the way to end of the guppies life, although it slows down considerably after seven months on average. The point is that the guppy color system is dynamic in space and time.

So what is the advantage of the Bagnara model for color cell layering versus the different forms of the Base Body System? It models the arrangement of the color cells in the skin more accurately. It defines the roles of the different classes of color cells more clearly. It provides a more comprehensive model for guppy colors. For example, colors like green (blue iridophore plus yellow pigment), purple (blue irodophore plus red pigment) or red metallic (silver iridophore plus red pigment) are modeled using the Bagnara system and not modeled by the Dzwillo system.

The Dzwillo system has not really been updated in the half-century since Dzwillo proposed it. It is still based on the two layer idea that the guppy has a base color and secondary sex colors are simply overlaid on top. People have added base and secondary colors to the system but they have not fundamentally changed its model of the color cells in the skin despite the work of Bagnara published in the decades after Dzwillo's 1959 paper.

Dr. Rick Squire sent me an interesting paper that was published in 1958 that explains the colorful morphs seen on betta splendens in terms of three layers of color cells. See "Genetics of the Siamese Fighting Fish, Betta Splendens"(Genetics. 1958 May; 43(3): 289–298) by Dr. Henry M. Wallbrunn. He divides the layers of betta color into a superficial layer of the scales, an intermediate area and a deep zone. His account of how our perception of betta color is influenced by the location of the color cells in the skin is different than that of Bagnara. For example, he places the iridophores above the yellow and red pigment cells, rather than below them.

Wallbrunn's view of way you have to think about fish color is nicely encapsulated in the way he describes his method for properly examining the color of bettas (p. 290)

If light is reflected from the iridocytes at an obtuse angle rather than approximately 90^o, green may look blue and blues look purplish. Hence the “correct” method of examination is to light the aquarium from the front. The “correct” criteria include classifying any specimen that shows green at any angle, green even though it may seem blue with other lighting since blue fish never appear green. Steel or dull blue is not easily confused with green or (bright) blue.

It is also interesting to note that Wallbrunn references the 1944 paper by Goodrich on the blond and golden genes (The cellular expression and genetics of two new genes in Lebistes reticulatus.) Obviously scientists consider a proper understanding of the way guppy color cells are positioned in the skin to be an important prerequisite to any study of color genetics.

The Fourth Dimension: Time and Color Cell Development

Bagnara's insight, that all color cells derive from a single precursor, has received important experimental support in the years since he proposed it. Today, we would say the color cell early in development is multipotent. Let me briefly explain what this concept means.

Life begins with the egg which is totipotent, meaning it can develop into any of the over 200 types of cells in the human body. But as soon as four days after fertilization cells begin to specialize. At that point they are said to become pluripotent meaning a bit more restricted in their ability to differentiate into different types. And after than they become multipotent meaning they are restricted to become a certain tissue type. In fish, the multipotent color cell is one that can develop into the different types of color cells, melanophores, xantho-erythrophores, leucophores, iridophores and cyanophores. So what makes a multipotent color cell develop as a melanophore (black color cell) instead of a leucophore (white color cell)? The process by which color cells become differentiated into the different types is called gene regulation. Color cells are under regulation from genes that promote or restrict their development.

In guppies, we can assume that faulty genes may prevent color cells from developing as a certain type or alternately encourage color cells to become a certain type. In fact it is usually the case there there are a number of different genes coming into play over time as a color cell develops. A good analogy to this is the way computers are programmed. Computer logic like "if a then b else c" governing whether a certain result occurs or not is analogous to the combinatorial logic of gene regulation systems. So whether or not a yellow or red color develops on a guppy as it matures might be the result of this kind of logic.

Biological Pathways

The focus of modern fish color and pattern research has shifted to understanding how color cells are specified, how they differentiate during development and the morphological changes they go through. Scientists recently (in the last thirty years) have acquired the tools for observing and documenting these changes on the molecular level. There is exciting research being conducted on Zebrafish color biology that shows color cells to be regulated in complex ways that affect where, how and when they are expressed. A leading researcher in this field, David Parichy, summarizes the situation in this way: "Understanding the development and evolution of pigment patterns requires knowledge of the cellular interactions and signaling pathways that produce those patterns." (Not just black and white: pigment pattern development and evolution in vertebrates. Seminars in Cell and Developmental Biology, doi:10.1016/semcdb.2008.11.012) You can download and read his paper at a repository for his lab. I highly recommend it.

What Parichy summarizes is the work that is being done to untangle the complex web of genetic factors affecting the development of color cells and their pigments or purine platelets. What the evidence shows is that colors like black are not the expression of a simple "black gene." Whether a color cell becomes a black color cell or a reflecting color cell (iridophore) is the final outcome of a cascade of cellular signals during development. How big it grows to is regulated by genes. How it interacts with other color cells are regulated by genes. There are products of many genes involved.

An illustration will show how dynamic this process is. This diagram from Wikipedia shows a cell (large rectangle) and nucleus (small rectangle) and the molecular signals processed by the cell.

Shown on the walls of the cell are receptors, a kind of listening post to chemical messages from other cells or messages that originate in the environment. The cell is literally being bombarded by signals during its development altering its shape, its size, its location on the body, the amount of pigment it produces and its relationship to neighboring cells.

Evaluating Dzwillo

Dzwillo was of course unaware of the complex systems behind guppy color and patterns. Gene regulation had only been proposed as a model in the early 1950s. He was working with a model that proposes that the base body colors have one kind of genetic basis and the secondary sex colors have another kind of genetic basis. But as you can see from the model of the cell and its signaling pathways, color cells are not organized into these two simple categories. Each color cell is an independent unit responding to developmental cues, conditions in the environment, internal instructions and so on. The colorful morphs you see in guppies are due to malfunctions in these signaling pathways.

I can summarize what I have said so far by saying that I consider Michael Dzwillo a true pioneer in the exploration of guppy color and pattern. His Base Body System was definitely a step in the right direction in terms of understanding the genetic basis for guppy color and pattern. But just like the work of Mendel, the field has moved forward and we now have a better understanding of how guppy color cells manipulate light (the Bagnara three dimensional color system) and we now have better models for understanding how color cells are specified, differentiate and change over time.

Evaluating the Base Body System in the Light of Modern Cell Biology

The four classes of color cells are present at birth. They further develop and become organized as the guppy sexually matures. The so-called base body colors don't exist apart from the secondary sex colors. To divide guppy color mutations this way just does not make sense from the point of view of contemporary color cell biology. Golden (called bronze in the U.S., tiger in Asia and gold in Europe) is a mutant black color cell that is larger than normal and distributed in the skin differently than normal color cells. Blond (called gold in the U.S. and Asia) is a mutation of a black color cell that is smaller than normal and has lost pigment motility. Albinism is a failure in the synthesis of black pigment. These are not base body colors, these are mutations affecting color cell development. Classifying them as the base colors a guppy is born with is not helpful in understanding how the mutation affects the Bagnara three dimensional color system.

The base body colors added in recent years just don't make sense as base body colors. Magenta, which is usually identified as a base body color, is a mutation affecting yellow or red which is usually considered to be a secondary sex color. Asian Blau (called R2 under the European base body system) is considered to be a base body color (blue) but it is actually a mutation that affects the development of red and yellow color cells. The Pink base body color affects red color cells, another secondary sex color. These mutations affect how color cells differentiate into color cell types and how they undergo morphological change. Their effect on a guppy's perceived color and pattern is more effectively modeled by the Bagnara Three Dimensional Color System. The Bagnara system does not artificially divide mutations between those that the guppy are born with and those that are under the influence of sex hormones. You can use it at any time during the guppy's development. The Bagnara system models how the light falling on a guppy is actually manipulated by the color cells. It is not based on the erroneous theory that colors exist in two layers, one acting as the background and the other the foreground.

The Bagnara system is probably too complicated and unwieldly to be used at guppy competitions so I am not recommending that the base body system be overthrown in its favor. I actually don't think guppy conformance shows need the base body system either. But that is for that community of guppy hobbyists to decide among themselves.