Homology: Integrating Phylogeny and Development
Marc Ereshefsky
Department of Philosophy
University of Calgary
ereshefs@ucalgary.ca
The importance of homology in biology is widely acknowledged. Wake (1994: 284) writes
that “[h]omology is the central concept for all of biology.” Paterson (1987: 18) observes that
“all useful comparisons in biology depend on the relation of homology.” Whenever we ask if
two characters are the same character we are asking if they are homologous, regardless of
whether those characters are genetic, morphological, anatomical, or behavioral. Yet like
many central concepts in biology, our understanding of homology is plagued by unresolved
questions. For example, how should we define ‘homology’? There is no agreed upon
definition in the literature. Or, how do we explain the fact that two homologous characters
can be caused by non-homologous developmental factors (Hall 2007)? Or more
fundamentally, what causes new homologues (Wagner 2001)? Then there are questions
about the role of homologies in evolution. Homologues are quasi-independent, heritable
units that selection acts on; they are units of evolvability (Laubichler 2000; Brigandt 2007).
The idea of homologues as units of evolvability cries out for analysis.
These are all pressing questions, but this paper will focus on just two of them. One is
the possibility of a unified theoretical account of homology. The other is how homologues at
one hierarchical level are caused by non-homologues at a lower level. As we shall see,
recent work offers an emerging approach to homology that integrates phylogeny and
development (Laubichler 2000). Such an approach provides the basis for a unified
theoretical account of homology, and it sheds light on the hierarchical nature of homology.
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Multiple Definitions
Just as there are multiple definitions of ‘species’ in the biological literature, there are
multiple definitions of ‘homology.’ And like the debate over species, there is no consensus
on the correct definition of homology. A partial list of prominent definitions of the last forty
years includes: the Transformational Homology Concept (Mayr 1969); the Operational
Homology Concept (Sneath and Sokal 1973); the Taxic Homology Concept (Rieppel 1992);
the Informational Homology Concept (Van Valen 1982); the Developmental Homology
Concept (Wagner 1989); and the Organizational Homology Concept (Müller 2003).
Among these definitions, the two most widely accepted approaches to homology are the
taxic and developmental ones. The taxic approach is found in the work of cladists and states
that a homologue is none other than a synapomorphy – a derived character that defines a
monophyletic group of organisms. Homologous characters have phylogenetic continuity:
they are genealogically connected to a common and unique ancestor. The developmental
approach to homology focuses on ontogeny rather than phylogeny. Two characters are
homologous if they share the same set of developmental constraints. Those constraints form
a developmental module (Wagner 1996). Such modules cause the stable production of a
homologue, yet are sufficiently independent from one another so that a change in one module
does not affect the efficacy of another module. Abouheif (1999) and Wagner (2007) suggest
that a homologue’s developmental module is a gene regulatory network consisting of the
genes and their interactions that cause the reoccurrence of a homologue.
Disagreement over the proper definition of ‘homology’ has caused some to be sceptical
of finding a unified theoretical account of homology. For example, Wake writes that “the
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homology debate is the result of biologists attempting to save an ancient, vague concept…
biologists should instead turn their attention to the questions that can be resolved” (2003:
193.) Maynard-Smith is reported as saying that ‘homology’ has “become a word ripe for
burning” (quoted in Tautz 1998: 17). Recently, Griffiths (2007) has argued that such
pessimism is unwarranted. Given that biologists have used the same operational criteria to
identify homologues for over 150 years and given that those criteria have spawned successful
research projects, we should think that homology is a natural relation. Nevertheless, Griffiths
remains pessimistic about there being a unified theoretical account of homology.
Hierarchical Disconnect
Another question about homology concerns its hierarchical nature. Consider four
hierarchical levels within individual organisms: genes, developmental processes,
morphological structures, and behaviour. Non-homologous factors at one level can cause
homologous traits at a higher hierarchical level. This is the phenomenon of hierarchical
disconnect. For example, in all tetrapods except newts and salamanders (urodele amphians),
primordial digits develop with tissue between them. At a later developmental stage, this
tissue dies off via apoptosis leaving tetrapod digits. In newts and salamanders the
development of digits takes a different path. Digits in those organisms develop separately,
and there is no need for apoptosis. Despite the different developmental processes responsible
for tetrapod digits, Hall (2003: 417) and others suggest that urodele digits and other tetrapod
digits are homologous. Here is a case where morphological structures are homologous, but
the developmental processes responsible for those structures are not homologous. Why is
there a hierarchical disconnect between this morphological structure and its developmental
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factors? The evolutionary hypothesis is that newts and salamander (or one of their
ancestors) lost the process of interdigit apoptosis, and the process of differential growth is a
derived condition. This type of explanation of hierarchical disconnect is common. New
genes substituted for old ones can cause the same homologous morphology (Abouheif 1999).
And, new morphological elements and movements can cause the same homologous
behaviour (Lauder 1994).
Hierarchical disconnect can go the other way too: homologous factors can cause nonhomologous characters. Eyes in vertebrates and compound eyes in arthropods are not
homologous (Abouheif 1997). Nevertheless, the homologous regulatory gene called Pax-6 in
mammals and eyeless in insects initiates the development of both kinds of eyes. Pax-6 (or
eyeless) has a single biochemical function, but that function is used differently in the
development of different characters (Abouheif 1997: 407). It is the same tool but put to
different uses in varying contexts. This phenomenon occurs among behaviours as well, where
non homologous behaviours rely on homologous morphological elements (Ereshefsky 2007a).
Towards a Unified Account
What are we to make of the multiple definitions of homology? How are we to understand the
phenomenon of hierarchical disconnect? There is an emerging unified approach to homology
that addresses both issues (as well as other issues). This approach is not new (Laubichler
2000), and it is found in recent work by phylogenetists (Rieppel 2005) and developmentalists
(Wagner 2007). This unified approach integrates ontogeny and phylogeny, and in doing so it
brings together the developmental and taxic approaches to homology. Furthermore, it is
consistent with some other approaches to homology. For example, this unified approach fills
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out the schema of the informational account (van Valen 1982) with a mechanistic account,
while at the same time dropping the reference to ‘information’ that some find problematic
(Wagner 1989). The motivation for such a unified account is simple. Homologies are the
result of both phylogenetic transmission and developmental mechanisms. So, a unified and
robust account of homology should cite both ontogenetic and phylogenetic factors. Here are
three important explanatory features that the taxic and developmental approaches bring to a
unified account of homology.
First, phylogeny is essential for establishing the identity conditions of a homologous
character. As many have pointed out, homology is a relation of sameness not similarity
(Müller 2003, Ghiselin 2005). As Owen famously wrote, a homologue is “[t]he same organ
in different animals under every variety of form and function” (1843: 379). Homologous
characters can occur in notoriously dissimilar character states. The forelimbs of humans,
dogs, bats, moles and whales are homologous. What causes similar and dissimilar character
states to be states of the same character? Phylogeny provides the identity conditions for
homology. Not in an operational sense, but in an ontological sense: the character states of a
homologue form a unique causal continuum, starting with the inception of that homologue.
Second, ontogeny is essential for explaining variation and similarity among the
character states of a homologue. Here we turn from the identity conditions for a homologue
to an explanation of the qualitative states of that homologue. Developmental modules, such
as gene regulatory networks, are the ontogenetic sources of both similarity and difference
among character states of a homologue (Abouheif 1999; Wagner 2007). The homologous
hind wings of butterflies and mosquitoes are similar in that they are appendages that occur on
the same part of the body. Yet the shapes and functions of those wings are quite different: in
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butterflies they develop as wing blades; in mosquitoes they develop as club-shaped sensory
organs. The gene Ubx is responsible for the development of the hind wings in both
butterflies and mosquitoes, and other genes cause variation among those wings (Wagner
2007: 474-475).
Third, developmental factors need to be transmitted across generations. Phylogeny
does that. But how does phylogeny contribute to the transmission of iterative homologues
within an organism, such as the bristles on the different legs of a fly? Historical homologies
occur in different organisms and are phylogenetically connected to a common ancestor.
Iterative homologies occur within a particular organism and are not obviously connected to a
common ancestor. In his earlier work, Wagner (1989) argued that the taxic approach to
homology was inadequate because it accounted for historical homology but not iterative
homology. Recently, Wagner has emphasised the need for a phylogenetic component in an
adequate account of homology: “Two genes are homologous so long as they are derived from
the same gene in a common ancestor” (Wagner 2007: 473). The phylogenetic transmission
of developmental mechanisms of iterative homologies occurs in two ways. First, the
developmental factors that cause instances of a single iterative homologue are
phylogenetically transmitted across generations. For instance, the developmental factors that
cause the bristles on the second leg of fruit flies are passed down from organism to organism.
Second, iterative homologues within an organism, such as the bristles on the second and third
legs of a fly, often trace back to a common phylogenetic origin (Strieder 1999: 40). As van
Valen (1982: 308) observed, genetic paralogues trace back to a common duplication event
and hence are phylogenetically connected. Hall (2003) and Gould (2002: 1061ff.) have
recently argued that a significant number of putative homoplasies may be phylogenetic
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homologues. Many parallelisms, they contend, are due to what some call ‘latent homology’
or ‘deep homology.’ Though at first it may appear that two characters evolved
independently, a closer look at the developmental factors that cause those characters reveals
that significant components of those factors trace back to a common ancestor. As Hall
(2003: 426) writes, “[t]his realignment of the categories of homologous and homoplastic
features provides a glimmer of a way to bridge the phylogenetic and developmental
approaches to homology.”
Moving away from these details, we see that a proper explanation of homology cites
both the developmental and phylogenetic causes of homology. And, recent work on
homology reveals the emergence of a modern theory of homology that integrates both kinds
of causes.
Integrating Hierarchical Levels
We have seen that homologies at one hierarchical level can be caused by non-homologous
features at a lower level. To explain the phenomenon of hierarchical disconnect we need an
account of homology that draws on both the phylogenetic and developmental approaches to
homology. Following the work of Minelli (1998), Wagner (1999), and Hall (2003), here are
four steps for investigating the phenomenon of hierarchical disconnect.
Because homologies occur at different hierarchical levels, the first step is determining
the level of a putative homology (Minelli 1998; Hall 2003). Is the putative homology
genetic, morphological, or behavioural? In the second step, phylogenetic analysis is used to
determine whether empirical evidence supports positing a homology (Hall 2003, Wagner
1999). Here such criteria as Remane’s (1952) and Paterson’s (1982) tests are used to
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distinguish homology from homoplasy. For example, Remane’s criterion of position says
that a structure’s occupying the same topographical position in different organisms is
evidence that it is a homologue. This and other tests for homology are often referred to as
‘operational.’ But this is misleading because such criteria are justified by theoretical
assumptions. While it is true that some of those tests, such as criterion of position, were used
to identify homologies prior to Darwin’s theory of evolution, their current use is supported
by theory. For example, evolutionary hypotheses explain why a homologue occupies the
same position in different organisms (Rieppel and Kearney 2007: 99-100; Rieppel 2007: 227228).
With phylogenetic evidence supporting the positing of a homologue, the third step
investigates the developmental mechanisms responsible for that homologue (Wagner 1999).
This step requires positing a model that explains the ontogeny of a homologue, and explains
the similarities and dissimilarities among its character states. For example, one might
investigate the gene regulatory network responsible for hind wings in butterflies. More
specifically, one might study which parts of that network are responsible for similarities in
hind wings and which parts are responsible for differences (Wagner 2007).
The fourth and final step integrates the developmental model of a homologue with its
posited phylogenetic distribution (Wagner 1999: 130-131). This final step brings together
two aspects necessary for explaining the occurrence of a homologue, namely the
developmental mechanisms responsible for a homologue and the phylogenetic transmission
of those mechanisms. In addition, a crucial test of a putative homologue is whether its
ontogenetic model and its phylogenetic hypothesis are congruent. If they are consistent, we
not only have an explanation of the homologue but further confirmation that the character in
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question is a homologue. If the ontogenetic model and phylogenetic hypothesis are
inconsistent, then something is wrong with either our explanation of the homologue or the
hypothesis that we are investigating a homologue.
As an example of this last step, recall the case of tetrapod digits. On the one hand,
phylogenetic evidence suggests that tetrapod digits are homologous. On the other hand,
evidence shows that the developmental mechanisms for digits in urodele amphibians differ
from the mechanisms in other tetrapods. In urodele amphibians, digits are the result of
differential growth; in other tetrapods, digits are the result of apoptosis between primordial
digits. The challenge is reconciling two different developmental explanations for tetrapod
digits with the phylogenetic hypothesis that all such digits are homologous. That involves
testing whether the developmental model and the phylogenetic hypothesis are congruent. As
we have seen, current work indicates that interdigit apoptosis is the ancestral process for digit
differentiation; urodele amphibians lost the process of interdigit apoptosis, and differential
growth in those organisms is the derived process. Here, then, we have a posited explanation
for why tetrapod digits are homologous though their developmental mechanisms are not.
The case of tetrapod digits shows how hierarchical levels within organisms can be
phylogenetically decoupled. At the level of morphology, there is the continuous lineage of
tetrapod digits. But at the level of developmental mechanisms, there is a bifurcating lineage
of developmental processes. The main branch of developmental mechanisms for tetrapod
digits consists of the process of apoptosis, while the process of differential growth is a
smaller branch growing off that main branch. Other examples of this sort of phylogenetic
decoupling are well documented. Gene substitutions in the genetic network of a
morphological homologue result in a branching phylogeny of genetic factors that cause the
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same morphological homologue (Abouheif 1999). Similarly, substitutions in the
morphological movements underlying a behavioural homologue result in a branching lineage
of movements that cause the same behavioural homology. For example, grasshoppers in the
genus Calliptamus produce a homologous song, but the morphological movements that cause
that song form a branching lineage of non homologous developmental factors (Striedter and
Northcutt 1991: 185-186).
Stepping back from these details, we see that explaining the phenomenon of
hierarchical disconnect requires investigating both the phylogenetic and developmental
causes of that phenomenon. Phylogeny explains transmission and identity; ontogeny
explains similarity and difference. Furthermore, a crucial test for the explanation of a
homology requires that the phylogenetic hypothesis and the ontogenetic model for that
homology are congruent (Wagner 1999).
Not so long ago, Wake pessimistically wrote: “I will grant that someone might be able
to generate an original thought concerning homology, but I doubt it” (1999: 24). He might
be right in that there are no new atomic thoughts concerning homology. But there is room
for optimism. Perhaps among the profusion of ideas concerning homology a synthesis of
some of those ideas may bring clarity and coherence to our understanding of homology.
The Metaphysics of Homology
One other aspect of the debate over homology is worth mentioning. Griffiths (1994),
Wagner (2001), Rieppel and Kearney (2007), and Brigandt (2007, in press) discuss the
ontological status of homologues, and they claim that homologues are natural kinds. On their
view, tetrapod digits are all members of the kind tetrapod digit. Grant and Kluge (2004) and
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Ghiselin (2005) disagree with this view of homologues. They argue that homologues are
parts of an individual rather than members of a kind. I think that Grant, Kluge, and Ghiselin
are right about the ontological status of homologues, especially in light of the integrated
approach to homology discussed in this paper. But before discussing why homologues are
parts of individuals, we need to be clear about the distinction between kinds and individuals.
The element gold is a paradigmatic kind. Pieces of gold are members of the kind gold
so long as they share certain similarities. Whether pieces of gold causally affect one another
does not matter when it comes being a member of the kind gold. The criterion for being the
part of an individual is different. Organisms are paradigmatic individuals, and the parts of an
organism must bear certain causal relations to one another. The tail and the nose of a dog
cannot be on different planets and be parts of a single dog; those parts must be causally
connected in certain ways. Whether those parts are similar or dissimilar is not essential for
their being parts of the same organism. Some philosophers have suggested that the
distinction between kinds and individuals is merely pragmatic (Boyd 1999). But this move
conflates different explanatory and classificatory practices in science and should be avoided
(Ereshefsky 2007b).
The integrated approach to homology discussed in this paper implies that homologues
are parts of individuals rather than members of a kind. An essential feature of homology is
phylogeny. Tetrapod digits, if they are homologous, must trace back to a common ancestor.
They must be historically connected and cannot be spatiotemporally scattered across the
universe. Furthermore, tetrapod digits need not be similar to be homologous. It is often
observed that homology is a relation of sameness not similarity. Even Owen’s (1843: 379)
famous quote that a homologue is “[t]he same organ in different animals under every variety
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of form and function” highlights this fact about homology. More recently, biologists draw
the distinction between characters and character states (Wagner 2007). This distinction also
highlights the distinction between the same homologue (character) and dissimilar
occurrences of that homologue (character states). Because being the same homologue does
not turn on qualitative similarity but historical connectedness, it is wrong to think that
homologues are kinds. The suggestion that homologues are best thought of as parts of an
individual should come as no surprise. After all, in this post-Darwinian era, historically
based explanations are essential for understanding the evolution of life. And, the relation of
homology as a historical relation plays a lynchpin role in those explanations.
Acknowledgements
I would like to thank Ingo Brigandt, Paul Griffiths, Jesse Hendrikse, Heather Jamniczky,
Elliott Sober, and Günter Wagner for their helpful comments on an earlier draft of this paper.
Thanks to Matt Haber and Joy Odenbaugh for organizing the Edges and Boundary workshop.
Financial support was provided by the Social Sciences and Humanities Research Council of
Canada.
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