Homology in the Age of Evo Devo: Part 1

Last week, I got to catch a talk and spend some time with Nicholas Holland, a biologist from the Scripps Oceanographic Institute at UC San Diego.  Dr. Holland discussed the history of the “homology” concept in science. Today, I want to start with a primer on the current debates regarding homology, and a little bit about the history of the concept. 

A Homology Primer

The textbook definition of homology is simple: homologies are characters that are shared by two organisms because they both inherited that characteristic from a common ancestor.  For example, the reason that humans, cats, and hedgehogs all have fur is because they share a furry common ancestor. Fur is a homologous trait among mammals.

However, it is not always so easy to determine what characteristics are really homologous.  Humans have complicated eyes, and so do octopi.  Are these structures homologous?:

Some aspects of these eyes are similar, for example they both have a lens and a retina. But some other characteristics are quite different. Human eyes develop as outgrowths of the brain, while octopus eyes develop from invaginations of the animal’s surface.  In humans, nerve fibers pass in front of the retina, creating a blind spot, while in octopi, the nerve fibers are behind the retina, so they don’t have that same limit to their vision.  These many differences, combined with the fact that many relatives of humans and octopi lack complex eyes, has led most scientists to conclude that human and octopus eyes evolved independently, or that they are evolutionarily convergent.

And the concept gets further complicated by the fact homology can vary depending on what level of organization you are talking about.  For example, the wings of bats and birds are convergent; each has independently evolved wings from an ancestor that had forelegs.  However, at the skeletal level the wings of birds and bats are homologous; they share the same bones in their wings (such the humerus) because the last ancestor of these animals had the same bones in its forelimb:

Homologies can exist at the genetic level as well. In the 1960’s, before genetics was well understood, many prominent scientists thought that animals gain and lose genes too quickly during evolution for homologous genes to exist (Dr. Holland had a great quote from the prominent, and in this case very wrong, biologist Ernst Mayr, “the search for homologous genes is quite futile except in very close relatives”).  We now know that most genes important to development are shared in animals as diverse as humans, fruit flys, and jellyfish. This discovery has been critical to biology, earning the 1995 Nobel Prize in Physiology or Medicine, and leading to the birth of evo-devo, but it has really complicated the idea of homology. The genes Pax6, Eyes absent, sine oculis, and dachsund form a network that is critical not only to the eyes of humans and cephalopods like octopi, but also the compound eyes of insects, which look nothing like our “camera-type” eyes. In fact, these genes are so conserved, that if a mouse has a faulty version of any of these genes, scientists can “rescue” eye development by injecting the mouse with the fruit fly version of the gene! Some evo-devo scientists have called this “deep homology”; that at the level of genetics these structures are derived from the same ancestral gene networks (e.g. Shubin, Tabin, and Carroll 1997).

But what does deep homology really mean?  In the 90’s many scientists took a very literal view.  If two animals shared an “eye” gene like Pax6, then their last common ancestor must have had Pax6 as well, and therefore an eye.  Many papers were using shared genes to construct complex animal ancestors (e.g. Arendt and Nubler-Jung 1996, De Robertis and Sasai 1996).  Dr. Holland included a great image of this idea in his talk, which was taken from Veraska et al (2000).  This shows the complex ancestor of humans, octopi, and frut flies, and the genes used to justify the complexity:

In the last decade, this idea has become hotly contested.  Some animals that do not share these complicated structures do share these genes, and some animals with these complex structures do not use the same genes to build them.  Currently, there is no consensus about what homologous genes tell us about the physical nature of the common ancestor.  I think this is the biggest question in evo-devo today. In my next post, I’ll go into detail on how Dr. Holland tackles this problem.

Papers Cited

Arendt, D. and Nubler-Jung, K. (1996). Common ground plans in early brain development in mice and flies. BioEssays 18, 255-259

De Robertis, E.M. and Sasai, Y. (1996). A common plan for dorso-ventral patterning in Bilateria. Nature 380, 37-40.

Mayr, E. (1963) Animal Species and Evolution. Harvard Univ. Press (p. 609)

Shubin, N., Tabin, C. & Carroll, S. (1997). Fossils, genes, and the evolution of animal limbs. Nature 388, 639–648

Veraksa, A, Del Campo, M. and McGinnis, W. (2000). Developmental patterning genes and their conserved functions: From model organism to humans. Molec. Gen. & Metabolism 69: 85-100.

How to Build A Snail

Raphaela Osterauer, Leonie Marschner, Oliver Betz, Matthias Gerberding, Banthita Sawasdee, Peter Cloetens, Nadine Haus, Bernd Sures, Rita Triebskorn, Heinz-R. Köhler. Turning snails into slugs: induced body plan changes and formation of an internal shell. Evolution & Development, 2010; 12 (5): 474

Osterauer et al. recently published a paper in the journal Evolution and Development where they were able to radically change the bodies of adult snails ( Marisa cornuarietis ) by exposing embryos to the metal platinum.

Snails, along with slugs, clams, octopi, and squid, are part of the group Mollusca (unsure of where the molluscs fit into the animal tree? Check the reference phylogeny).  Molluscs share a basic bodyplan, although it has been highly modified in different groups.

Snails, for example, develop their shells through a bizarre developmental process called torsion.  During torsion, multiple parts of the body are rotated 180 degrees.  By the end, the anus and gills are sitting above the head of the animal, the nervous system has turned into a figure 8, and the right and left hand sides of the animals have become assymetrical:

While scientists don’t entirely understand why torsion occurs, it is related to the growth of the external shell and the muscles that attach to it.  In other species of molluscs, such as cephalopods (octopi, squid, cuttlefish), nudibranchs (sea hares), and pulmonate slugs, torsion never occurs.  Instead, the shell grows inside of the animal, creating a cone-shaped internal shell. The cuttlefish bone, which is often sold in pet stores as a calcium supplement for birds, is an example of this internal shell.

While trying to study the effects of certain toxic metals on the snail M. cornuarietis, Osterauer et al. found that exposure to platinum led some snails to loose their shells.  In this study, the scientists discovered that when M. cornuarietis embryos are exposed to a concentration of 164.4 milligrams of platinum per liter during the fourth and fifth days of development, the mantle tissue stays inside of the body (at this level of platinum, 100% of animals tested had this result).  In a normal snail, the mantle tissue moves to the outside of the animal, and is responsible for secreting the chemicals that harden into a shell.  In the image below, the edge of the mantle tissue is stained black and pointed out with an arrow; notice the difference between the normal snail embryo on the left and the platinum-exposed embryo on the right:

So instead of forming a normal shell, the shell developed within the body, like one might find in a squid or slug. These shells developed cone-like shapes that are reminiscent of those found in mollusks that lack external shells. Below are photos of adult shell-less snails, with images of their internal shells superimposed to show size and location:

Without normal shell-formation, the gills and mantle tissue stay in the posterior end of the animal like in other molluscs.  The gut, however, still goes through torsion, with the anus moving into the anterior region.

The fact that they recovered similar results from a second, distantly related snail, Planorbarius corneus, increases the possibility that the authors have discovered an important aspect of snail torsion, as opposed to an anomaly restricted to Marisa cornuarietis.

Here are the points I think are important in this paper:

1) This study does NOT suggest that platinum was responsible for the evolution of snails into slugs and cephalopods (or vice versa).

Because platinum is not having any effect on the DNA of the snails, they cannot pass these changes on to their offspring.  If a change is not heritable then it cannot be important to evolution in the long term. 

2) What this work does suggest is that a small change in development plays a huge role in the design of a snail.

The most important point of this paper is that one change, the position of the mantle tissue, affected many attributes of the snail, including the shape of the shell, the position of the shell and the position of the gills.  Instead of each of these characteristics having to evolve independently in the evolution of snails into slugs and cephalopods (or vice versa, the evolutionary history of the molluscs is still not well known), one change in development could affect all of these attributes at once.

While platinum exposure almost certainly was not responsible for this evolutionary change, the platinum is probably disrupting a gene network that is important to snail torsion.  If scientists can determine which gene(s) are involved in this change, they might discover how natural mutations in snail DNA led to the same results as the platinum exposure. Hopefully this work will be followed up on by these researchers.  In fact, Osterauer et al. already have an educated guess that the platinum might be disrupting a Calcium-based positioning system, although the authors did not find any significant difference in calcium uptake between experimental and control animals.