Defining "homology"

Understanding why certain sorts of similarities stretch across large swaths of the biological world is a question that has fascinated biologists since before evolution provided a unifying theme for biology. It is hardly surprising that explanations drawn from the pre-evolutionary thinking of the early 19th century would have flaws in the modern evolutionary context. "Homology" is one such concept, and biologists debate the meaning and significance of that particular term because of its historical baggage. To clarify discussions of similarity and difference in an evolutionary context, biologists have coined new terms which avoid the confusions that Explore Evolution's chapter on homology chooses to wallow in.

The central error in the homology chapter lies in the authors' narrow focus on that particular word, rather than discussing the more modern concepts that scientists actually use to study morphological similarities and differences. The focus on outmoded terminology will only confuse students, a result which may not be inadvertent. It is doubly troubling that the chapter about homology never offers a definition of the term, and the attempts made at describing its scientific usage are simply wrong. Despite leaving the word's definition up in the air, EE repeatd the erroneous creationist canard of claiming that homology's definition is circular. The supposed circularity is simply a reflection of the authors' inaccurate presentation of the concept they are writing about, and the claim that an unspecified definition of homology is circular strains credulity in any event.

Unlike Explore Evolution, biologists do not treat homology as if each part of an organism existed in isolation. The pattern of similarity in genes controlling eye proteins reflect the same evolutionary history as the shape of bones in the leg and the genes controlling the development of the embryo. Biologists compare dozens, hundreds, or even thousands of different traits in many different species to develop a model of the evolutionary history of the group. With that model, they can test whether a structure is shared by two species because of shared evolutionary history, or because of shared selective pressures. This process of building a hypothesis, making predictions, and testing those predictions against data is critical to scientific inquiry, and its absence from Explore Evolutionfurther belies the book's claim to be inquiry-based. Its erroneous treatment of homology belies any claim that it accurately explores evolution.

Homology and similarity

Summary of problems:

Despite using the term in the title of two chapters, and using the word "homology" or "homologous" over 80 times, EE never provides a clear and consistent definition of homology. Their usage is inconsistent and vague, promoting confusion and obscuring the actual ways in which scientists use the term. Furthermore, the focus on "homology," as opposed to terms and concepts with clearer meanings and less historical baggage, introduces confusion to the discussion of the morphological evidence of common descent.

Full discussion:

In the glossary, "homologous structure" is [mis]defined as "a body part that is similar in structure and position in two or more species but has a different function in each; for example, the forelimbs of bats, porpoises and humans" (EE, p. 146). "Molecular homology" is defined in the glossary as "similarity of the nucleotide sequences of DNA or RNA molecules, or the amino acid sequences of proteins." In the text of this chapter, homology is never explicitly defined, but is referred to in the context of "similarities," without any restrictions regarding function. As discussed below, similarity of developmental pathways is treated as a requirement of anatomical homology, but is not included in any definitions. None of these definitions match the actual way scientists define and use the term homology, let alone how scientists evaluate the anatomical evidence for common descent.

To choose a trivial example, evolutionary biologists agree that the hooves of a cow and the hooves of a deer are homologous. By the definition EE offers, they could not be homologous structures since they share the same function. Badly misdefining the term that is central to two chapters, and then using it inconsistently throughout, is not a good way to increase student comprehension.

The glossary in Futuyma's Evolutionary Biology defines homology as "Possession by two or more species of a trait derived, with or without modification, from their common ancestor." West-Eberhard defines it as "similarity due to common descent," but adds that "homology, like 'fitness' and 'species', is an elusive concept. There is unceasing debate within evolutionary biology regarding its meaning and use" (M. J. West-Eberhard, 2003, Developmental Plasticity and Evolution Oxford University Press:Oxford. p. 485 of 794).

While the first mistake Explore Evolution makes in this chapter is its failure to define "homology" (correctly), the far greater error is that they do not engage with the ways that modern evolutionary biologists use the concept, and the ways in which the term "homology" has been superseded by clearer concepts.

Here is how biologist Günter Wagner explained the situation in 1989:

Among evolutionary biologists, homology has a firm reputation as an elusive concept. Nevertheless, homology is still the basic concept of comparative anatomy and has been used successfully in reconstructions of phylogenetic history. A large number of characters are certainly derived from the same structure in a common ancestor and are therefore undoubtedly homologous. One simply cannot escape the conclusion that the brain of a rat and a human are actually the "same" in spite of their obvious differences.
G. P. Wagner (1989) "The biological homology concept." Annual Review of Ecology and Systematics. 20:51–69

The phenomenon is real, but teasing out how to identify "homology" has proven difficult. As EE mentions, "homology" was originally coined by Robert Owen to describe a sort of Platonic ideal which individual species drew upon to produce their forms. This non-evolutionary treatment of the concept can promote confusion when thinking about a structure that evolved in stages, and various of those stages are still present. For an example, see our discussion of eye evolution below.

A term that many scientists prefer is "synapomorphy," or "shared, derived characteristic." This concept was crafted by Willi Hennig specifically to describe a trait of an organism which is shared by all of the descendants of a common ancestor, and which is not shared with other groups — it is newly derived within that lineage. Examining the pattern of shared, derived traits allows scientists to develop hypotheses about common descent, and examining additional traits allows scientists to test those ideas.

Tetrapod limbs provide an example of the way that scientists develop and test hypotheses about synapomorphy. Many different aspects of tetrapod limbs unite tetrapods as the descendants of a species like Tiktaalik (discussed in the critique of chapter 3). Such a species possessed certain novel traits that were passed on to their descendants. Within the various lineages, those traits changed, and those changes were passed on to their descendants. Using only synapomorphic concepts, we can make the following observations and hypotheses:

  1. Observation: Bats, seals, and birds are tetrapods (have four limbs) and the particular bones in their limbs share many of the same traits.
  2. Hypothesis: Bats, seals, and birds share a common ancestor.

  1. Observation: Bats share more limb traits with seals than they do with birds. The limb traits that bats share with birds are the same traits that seals share with birds.
  2. Hypothesis: The common ancestor of bats and seals is more recent than the most recent common ancestor of bats, seals, and birds.

The examination of limb morphology allows scientists to propose an hypothesis about the evolution of the groups which possess those limbs. That hypothesis can be tested by examining other traits, such as skull morphology, or DNA sequences. The hypothesis of common descent allows scientists to predict that the hierarchal arrangement of novel traits in each part of the organism should match the pattern derived from the other parts. Hypotheses about the synapomorphy of a trait can be tested by examining that trait in additional species which share the same common ancestor, as discussed below in the context of eye evolution.

By omitting any discussion of the way that scientists propose and test evolutionary hypotheses, Explore Evolution obscures the ways in which scientists actually use concepts like "homology" and "synapomorphy." Misdefining "homology" in the glossary is bad scholarship or an attempt to further confuse the issue at hand.

Homologous structures, genes, and developmental pathways

Summary of problems with claim:

Similarities in developmental pathways are one of several criteria scientists use for "homology." Presenting it as the sole criterion is incorrect.

Full discussion:

As noted elsewhere, the authors of Explore Evolution first create a "strawman" in generating their "Case For". Specifically, for anatomical homology, the authors draw the following conclusion: two different animals can be said to have "homologous structures because they were built by homologous genes" through "developmental pathways" that are homologous (p. 41). To add support to their conclusion, the authors quote two "neo-Darwinian biologists" Alfred Romer and Thomas Parsons who believed "[T]he identity between homologues is based upon the identity or similarity of the developmental properties…[and] hereditary units, the genes" (EE, p. 41). The source cited is a textbook originally published in 1949, with the latest edition published in 1977. Biologists’ understanding of genes and development has advanced dramatically in the past 30 years, and it is irresponsible of the authors to rest their discussion on such an outdated source.

Closer examination of the "Case For" reveals many problems with assuming the above conclusion. Darwin did not know about genes and developmental pathways. Darwin’s theory of common descent and thoughts regarding homologous structures make no predictions about what we expect to find at the developmental and genetic level. Numerous evolutionary biologists have addressed this assumption. Wagner (1988) stated that there is no simple congruence between anatomical characters and genotypes and hypothesized that only those features of the developmental system that cause a restriction in the possible phenotypic consequences of genetic variation (i.e., developmental constraints) are important. Even de Beer (1951), quoted by the EE authors as a critic of anatomical homology, believed that "the homology of phenotypes does not imply the similarity of genotypes".

Certainly, similarity in developmental control can be helpful in establishing structures as homologous (similar in structure and position as the result of common ancestry). Development, however, is far more complex than the EE authors would have their readers believe.

Developmental plasticity plays a major role in our modern understanding of biology and evolution. Processes such as the change in timing or location of developmental events may lead to changes in size and shape, and may alter the relationship between a developmental pathway and morphology without altering homologous relationships. In general, variations in the expression of a gene (late versus early, prolonged versus brief, constant vs. intermittent, spatially contiguous vs. discrete locales) can influence developmental and phenotypic outcomes.

Mindell and Meyer (2001) point out that reticulate (lateral) evolution and the dissociation among traits at different hierarchies (e.g. genes, morphology, development) can result in genes having complicated histories. Orthology, paralogy, and xenology all describe similarities between genes that arise from processes of organismal lineage splitting, gene duplication, and horizontal transfer of genetic material, respectively. The dissociation of traits can result in the co-option of genes for different functions. For instance, Mindell and Meyer (2001) hypothesize a dissociation has occurred between the developmental mechanisms and the digit primordia in the avian hand. In theropods, developmental mechanisms acted on primordia 1-3, whereas the same mechanisms act on primordia 2-4 in birds. Mindell and Meyer (2001) argue this might explain why the digits do not appear to be phylogenetically homologous in theropod dinosaurs and birds, in conflict with many other characters that suggest they are sister taxa.

The issue is not whether homologous structures exist, but why developmental and genetic processes inadequately account for homology. The authors of Explore Evolution want you to believe that the lack of correspondence between some phenotypic structures hypothesized to be homologous and genetic\developmental pathways underlying these structures is evidence against common ancestry. Recent scientific research in evolutionary developmental biology (evo-devo) is providing data in support of other, more parsimonious, and even wondrous, explanations, as well as proposals of new terms such as homocracy, to describe organs/structures which are organized through the expression of identical patterning genes. Hence, many homologous structures are in all probability homocratic, whereas only a small number of homocratic structures are homologous. And while intuitively one might expect that the historical continuity of morphological characters should be underpinned by the continuity of the genes that govern the development of these characters, Wagner (2007) points out that things are not that simple. Instead, regulatory networks of co-adapted transcription factor genes may be more important in orchestrating the development of homologous characters.

In a major work synthesizing developmental biology and its effects on evolution, Mary Jane West-Eberhard lists various major criteria which have been used to propose homologous relationships. These include "similarity in position and structural detail"; "presence of connecting intermediates or transitional forms, including in ontogeny [development]"; "similarity in development, taken to mean shared developmental pathways, shared developmental constraints, or evoked by the same stimuli"; "lack of conjunction, or lack of coexistence in a single organism"; or "genetic similarity" (M. J. West-Eberhard, 2003, Developmental Plasticity and Evolutionary Biology, Oxford University Press:Oxford, p. 489 of 794, references and quotation marks omitted).

Any of these criteria can be applied in a given situation, depending on the information available and the interests of the researcher. West-Eberhard observes:

As pointed out by Donoghue (1992) "The choice of a [specialized] definition is, at least in part, a means of forcing other scientists to pay closer attention to whatever one thinks is most important" (p. 174). It also invites endless argument over what the "correct" definition should be. The choice of criteria is partly a pragmatic matter. The most powerful procedure is to recognize that there are numerous criteria, and given the difficulty of tracing homologies, as many as possible should be used.
Mary Jane West-Eberhard (2003) Developmental Plasticity and Evolutionary Biology, Oxford University Press:Oxford, p. 489 of 794, and quote from Donoghue (1992), "Homology" in Keywords in Evolutionary Biology, E. F. Keller and E. A. Lloyd (eds.). Harvard University Press: Cambridge, MA, pp. 170-179.

These criteria are the ground for initially proposing homology, but are not the final step. The scientific process rests on repeated inquiry and testing, using new lines of evidence to test the evolutionary history of a lineage, and to understand the detailed history of a particular structure. Developmental pathways are one line of evidence examined, but are not the only basis for identifying homology, nor for testing a hypothesis of homology. Explore Evolution fails here by misleading students about the way scientists assess homology and by misrepresenting the scientific method of proposing and testing hypotheses.

Circular definitions

Summary of problems:

This claim has a long history in the creationist literature, but is uniformly rejected by biologists as rooted in basic misunderstandings. The apparent homology of a single trait would not be treated as evidence of common descent. By examining multiple traits, all showing the same nested hierarchy of modifications of a common starting point, scientists can test hypotheses about common descent. There is nothing circular about this process.

Full discussion:

The argument that homology is defined in a circular manner was a centerpiece of Jonathan Wells's creationist book Icons of Evolution. Wells, an uncredited co-author of EE, undertook graduate studies in biology at the behest of his religious leaders. He explained to a Unification Church ("Moonie") publication "Father [Sun Myung Moon]'s words, my studies, and my prayers convinced me that I should devote my life to destroying Darwinism."

EE reuses Wells's figure 4.1 as its figure 2:1, merely adding color to the figure. Similarly, the discussion of homology as a circular argument is a lightly rewritten version of what Wells wrote. Compare EE:

Some biologists suggest that the problems of understanding homology stem from Darwin himself, who re-defined homology as the result of common ancestry.

This made the concept of homology circular, say many critics. If homology is defined as "similarity due to common descent," then to say that homology provides evidence for common descent is to reason in a circle.
EE, p. 49

Wells writes:

before Darwin (and for Darwin himself), the definition of homology was similarity of structure and position …. But similarity of structure and position did not explain the origin of homology, so an explanation had to be provided.

But for twentieth-century neo-Darwinists, common ancestry is the definition of homology as well as its explanation.

[E]volution was a theory, and homology was evidence for it. With Darwin's followers, evolution is assumed to be independently established, and homology is its result. The problem is that now homology cannot be used as evidence for evolution except by reasoning in a circle.
Jonathan Wells (2000) Icons of Evolution, Regnery Publishing, Inc.:Washington, DC. pp. 62-63

The restatement of these claims in EE does not require any different response than Wells received, since it adds nothing to the argument. Reviewer Alan Gishlick responded to Wells's treatment of homology:

Wells claims that homology is used in a circular fashion by biologists because textbooks define homology as similarity inherited from a common ancestor, and then state that homology is evidence for common ancestry. Wells is correct: this simplified reading of homology is indeed circular. But Wells oversimplifies a complex system into absurdity instead of trying to explain it properly. Wells, like a few biologists and many textbooks, makes the classic error of confusing the definition of homology with the diagnosis of a homologous structure, the biological basis of homology with a procedure for discovering homology. In his discussion, he confuses not only the nature of the concept but also its history; the result is a discussion that would confuse. What is truly important here is not whether textbooks describe homology circularly, but whether homology is used circularly in biology. When homology is properly understood and applied, it is not circular at all.

Today, biologists still diagnose homologous structures by first searching for structures of similar form and position, just as pre-Darwinian biologists did. (They also search for genetic, histological, developmental, and behavioral similarities.) However, in our post-Darwin period, biologists define a homologous structure as an anatomical, developmental, behavioral, or genetic feature shared between two different organisms because they inherited it from a common ancestor. Because not all features that are similar in two organisms are necessarily inherited from a common ancestor, and not all features inherited from a common ancestor are similar, it is necessary to test structures before they can be declared homologous. To answer the question, "could this feature in these groups be inherited from a common ancestor?" scientists compare the feature across many groups, looking for patterns of form, function, development, biochemistry, and presence and absence.

If, considering all the available evidence, the distribution of characteristics across many different groups resembles a genealogical pattern, it is very likely that the feature reflects common ancestry. Future tests based on more features and more groups could change those assessments, however — which is normal in the building of scientific understanding. Nevertheless, when a very large amount of information from several different areas (anatomy, biochemistry, genetics, etc.) indicates that a set of organisms is genealogically related, then scientists feel confident in declaring the features that they share are homologous. Finally, while judgments of homology are in principle revisable, there are many cases in which there is no realistic expectation that they will be overturned.

So Wells is wrong when he says that homology assumes common ancestry. Whether a feature reflects common ancestry of two or more animal groups is tested against the pattern it makes with these as well as other groups. Sometimes, though not always, the pattern reflects a genealogical relationship among the organisms — at which point the inference of common ancestry is made.

Evolution and homology are closely related concepts but they are not circular: homology of a structure is diagnosed and tested by outside elements: structure, position, etc., and whether or not the pattern of distribution of the trait is genealogical. If the pattern of relationships looks like a genealogy, it would be perverse to deny that the trait reflects common ancestry or that an evolutionary relationship exist between the groups. Similarly, the closeness of the relationship between two groups of organisms is determined by the extent of homologous features; the more homologous features two organisms share, the more recent their common ancestor. Contrary to Wells's contention, neither the definition nor the application of homology to biology is circular.

Some formulations of the concept of homology appear to be circular, but as discussed above, because there is an external referent (the pattern that characteristics take across groups) that serves as an independent test, the concept, properly defined and understood, is not. Wells's claim that homology is circular reveals a mistaken idea of how science works. In science, ideas frequently are formulated by moving back and forth between data and theory, and scientists regularly distinguish between the definition of a concept and the evidence used to diagnose and test it.

Gishlick here is using "homologous features" in the sense of a "shared derived character," as discussed above. There are several important points that bear emphasizing.

First, biologists do not look at only one line of evidence to infer common descent; it is the agreement of multiple lines of evidence about morphological, genetic, behavioral, ecological and developmental similarity which allows that inference.

Second, that inference is a testable hypothesis. The addition of new lines of evidence allows a test of evolutionary hypotheses. For instance, biologists will test evolutionary hypotheses produced based on skull morphology with information from the DNA sequence of a particular gene. A common test for the accuracy of an evolutionary inference is to run the same analysis while excluding part of the data, and using those excluded data to confirm the accuracy of the results.

Third, the hypothesis of homology (which follows from an evolutionary hypothesis) is testable. In reconstructions of the common ancestry of a group, it is not uncommon to find that certain traits evolved more than once, or appear and disappear at various points on the tree. Those characters are then subject to greater scrutiny, since their disagreement with other traits suggests that there may be more that needs to be understood about that trait. Some traits which appear similar are deemed not to be homologous as a result of this analysis, but to be the result of parallel evolutionary pressure.

Fourth, the evolutionary hypothesis can be tested by reference to previously unexamined species. If the evolutionary hypothesis is correct, new species ought to fit easily into the pattern predicted. Since the evolutionary hypothesis is based on nested groups sharing certain novel traits, that hypothesis would be challenged if newly described species had a mosaic of traits that did not fit into that nested hierarchy.

Explore Evolution, like other creationist books before it, makes the mistake of treating the structures of organisms in isolation. While it would be circular to use a single trait to infer an evolutionary history and then to use that history to infer the common ancestry of that trait, scientists do not do that. In presenting homology and common descent as a circular construct misused by scientists, EE misinforms students about basic concepts, bringing confusion rather than clarity.

Scientists build on earlier hypotheses with new data, and build new hypothesis from that new data. This advance in knowledge adds a third dimension to what EE treats as two-dimensional. Rather than a flat circle, the scientific process spirals upward.