On Homology

Richard Owen, one of the great fathers of paleontology, is a curious figure in the history of biology. A contemporary of Darwin’s, he had ambiguous and sometimes self-contradictory views of evolution. Nevertheless, his most lasting contribution to modern biology is the concept of homology, one of the guiding principles of evolutionary biology.

Owen noticed that the limbs (for example) of bats, cats and seals all had a common plan – a single humerus followed by a pair of parallel bones called the radius and ulna, two rows of pebble-like bones called carpals and then a system of  long, thin bones called metacarpals and phalanges – even though they had very different functions and outward appearances. As a result, he drew a distinction between two different kinds of anatomical similarity. When two organs are similar only in function, but not in appearance, he said that their relationship was one of “analogy.” But when two organs were similar because they fit into the same plan, he called the relationship “homology.” The bat wing, cat paw and seal flipper are homologous with each other, but a bird’s wing and a fly’s wing are analogous.


The limbs of a human, dog bird and whale, color coded to show homologous bones. Courtesy Wikimedia Commons.

Oddly, although he knew Darwin’s work very well, and although the concept of homology is now explained in terms of evolutionary relationships, Owen maintained that homology only reflected the common designs in the mind of the Creator. Today, we have a different view: homology is defined as similarity as a result of separate descent from a common ancestor. The bat, the cat and the seal all had a common ancestor whose arm-bones were laid out in the same way as its descendants’.

The concept of homology is both crucial to evolutionary biology and maddeningly ambiguous (somewhat like Owen himself). It is crucial because if we want to ask essential questions such as, “how did birds evolve wings?” we must necessarily talk about homologous structures in the ancestors of the birds. But it is ambiguous for a host of practical and philosophical reasons.

The problem is that any single case of homology is difficult to prove. Even when the similarities are obvious, there is a fundamental problem: how do we know that what we see isn’t a product of convergent evolution, or just of chance? After all, the ancestor-descendant relationship isn’t something we can see or touch. My hand may be a homologue of a cat’s paw, but we cannot see a physical connection between them. My hand didn’t even exist during the early stages of my embryological development, so there is a definite discontinuity between my hand and my ancestors’ hands. In what way can we call them “the same”?

The above argument may sound like a philosophical quibble, but rest assured the biological literature is littered with arguments about whether various organs are homologous with each other. These debates could not arise if homology were something we could just point to. See this thumb? We know it’s homologous to that bat’s little finger because there is a piece of homology-string connecting the two. It just doesn’t work that way.

A paper was released recently (Icardo et. al 2016), in which the authors suggested that part of a hagfish’s heart is not homologous to a similar part found in the hearts of other fish. This is particularly interesting to me as a professor of human anatomy because the part in question, the sinus venosus, is believed to be homologous to the natural pacemaker of our human heart, the sino-atrial node. Fish have a four-chambered heart, with all four chambers forming a sort of chain: first the sinus venosus, then the atrium, then the ventricle and finally the “OFT” or outflow tract. Blood flows into the sinus venosus, which contracts, sending the blood to the next chamber, which then contracts and so on until the blood is pumped out ofthe heart. Lamprey and hagfish are interesting because although they are aquatic vertebrates, they aren’t really fish. If you like, you can call them jawless fishes, but that doesn’t really help. The fact is, they represent a lineage of vertebrates that split off before the evolution of jaws. So, they retain some ancient chordate characteristics that “true” fish have lost. In some ways they are more like sea squirts than like jawed fish.

So, these scientists looked at the hearts of lampreys and hagfish in order to understand the evolution of the heart. They found what looks like a four-chambered pattern, but one of the chambers – the sinus venosus – looked odd under the microscope and it plumbed into the heart from a strange direction. They had to ask themselves whether it is actually homologous to the sinus venosus of the fish heart. Based on anatomical considerations, they concluded that it isn’t.

There is another homology debate that has burned slowly for decades: the relationship between feathers, hairs, and scales. Birds, mammals, and reptiles are all examples of a large group of organisms called amniotes. All amniotes evolved from a common ancestor who was adapted to live on dry land. Amniotes have a structure called the amnion in their eggs to prevent water-loss (mammals maintain an amnion in utero, even though we don’t have eggs), and they have a water-proofing protein in their skin called keratin.

Our hair is made of keratin, as are birds’ feathers and reptiles’ scales. But are they really homologous with each other? (Fish scales are totally different, btw. They are made of a bone-like material) Here’s the problem: scales, feathers and fur all seem to form by folding of the epidermis (the skin’s outer layer, and the one that makes keratin), but they fold in different ways. In birds and mammals, the epidermis first forms small thickened spots called placodes. The placodes then form outward extensions (that become feathers in birds) or inward growths (which, in mammals, sort of forms a chamber that extrudes keratinous hairs). Reptile scales seem to form without placodes. Instead, small regions of the epidermis become elevated without thickening, and then fold back on themselves to form the scales. The differences seem subtle, but they are crucial – again, because of our earlier philosophical quibble.

As I said before, homology is similarity by means of common descent. However, the homologous organ itself does not descend from generation to generation; only DNA is actually inherited. The way out of this conundrum is simple: the DNA defines for a developmental program that produces the organ in each generation. So, one excellent way to test a hypothesis of homology is to look at the developmental process that produces it. According to that rationale, if lizard scales and bird feathers grow from different structures, we can’t say they are homologous. Ditto scales and hairs. So, bird feathers are homolgous with mammal hairs, but neither is homologous with scales. Right?

Sigh. Not so fast. Birds are descended from reptiles! Take any lizard or crocodile and any bird, and their common ancestor occurred much later than the common ancestor between mammals and either birds or reptiles. What we wanted to see was a homology between feathers and scales, and confirmation that hairs are somehow different. Thus, endless debate ensued, with lots of conjectural explanations.

Enter Nicolas Di-Poï and Michel C. Milinkovitch (2016). They decided to take a closer look, and they used (a) more modern techniques and (b) a mutant lizard.

By carefully observing reptile skin, they were able to confirm the previously understood mechanism of scale development: elevated regions that fold over to become scales. However, they also found small placodes. They argue that these placodes had been missed in previous studies because they appear and disappear quickly, and on different parts of the body at different times. However, they confirmed that the placodes do produce the same sorts of signaling compounds (morphogens) seen in the production of feathers and fur. In other words, the placodes do exist and they do have the right kind of effects on the surrounding tissues. We can say that they do cause scales just as they cause feathers and fur. But that wasn’t enough for them.

It seems that there is a breed of bearded dragons that have no scales, just comparatively smooth skin. The authors identified the mutation that causes scaleless lizards. It occurs in a gene already known to be important for the signaling pathway that causes the production of feathers and hairs, and which they showed was present in normal lizard scales. Actually, their work was already pretty convincing without the second part – but who could resist the temptation to do an experiment on scaleless mutant lizards?

There is a lot more to say about homology. we’ve developed dozens of types since Owen’s time: molecular homologies, serial homologies and so forth. But we’ve found a resolution to one homological problem. Perhaps that’s enough for one day.
Cited Literature

Nicolas Di-Poï and Michel C. Milinkovitch, 2016. The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes. Sci. Adv. 2, e1600708.

Jose M. Icardo, Elvira Colvee, Sarah Schorno, Eugenia R. Lauriano, Douglas S. Fudge, Chris N. Glover, and Giacomo Zaccone, 2016. JOURNAL OF MORPHOLOGY 277:853–865.

For more information, check out Michel Milinkovitch’s site: http://www.lanevol.org/


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