Homology is a concept that is fundamental to biological studies, and yet it is difficult to define. Generally, characters are considered to be homologous among organisms if they have been inherited from a common ancestral character.
Homology is thus at the heart of phylogenetics, as it expresses the historical relationships among characters, whereas a phylogeny expresses the historical relationships among taxa (including individuals). Since the relationships among the taxa are based on pre-existing information about the relationships among the characters, homology must be established first. It is for this reason that multiple sequence alignments, for example, are so valuable.
However, homology is a relative concept; that is, it is context sensitive. It only applies locally, to any one level of the hierarchy of character generalization. The classic example of this idea is bird wings versus bat wings. These structures are homologous as forelimbs but not as wings – birds and bats independently modified their forelimbs into wings. So, homology exists at the more general level (forelimbs) but not at the less general level (wings). Forelimbs developed first in evolutionary history (the common ancestor of animals with four legs is ancient), and later these forelimbs were modified in different descendants, with some developing wings, some flippers, and some arms. Wings, flippers and arms are more recent, and are thus less general.
So, we can conceptualize characters as existing at many hierarchical levels of generality, depending on when they developed. We might have (going from specific to general) nucleotides, amino acids, protein domains, proteins, biosynthetic pathways, developmental origins, and anatomy, among many possible conceptual levels. Lower levels in the hierarchy "control" the upper levels, so that nucleotides code for amino acids, domains consist of strings of amino acids, proteins function as enzymes in biosynthesis, and development is controlled by biosynthetic pathways.
|A nucleotide insertion and compensatory deletion results in two amino acid substitutions,|
so that simultaneously aligning homologous nucleotides and homologous amino acids is no longer possible
The issue is that homology among characters can only be determined within any one hierarchical level. As noted by Fitch (2000): "Life would have been simple if phylogenetic homology necessarily implied structural homology or either of them had necessarily implied functional homology. However, they map onto each other imperfectly".
For example, homology of amino acids among a group of organisms does not necessarily imply that all of their coding nucleotides are homologous (see the figure above) — originally the nucleotides would also have been homologous, but insertions and deletions through time can break the original relationship between the amino acids and their coding nucleotides. So, one cannot always simultaneously align homologous amino acids and homologous nucleotides.
Similarly, homology of two anatomical features does not necessarily imply that their developmental sequences are homologous. This is an issue that the study of evo-devo has made increasingly obvious. That is, sometimes identity of morphological characters is not the result of identity of the sets of genes that control their development (Meyer 1999; Mindell and Meyer 2001; Wagner 2014) — non-homologous genes and gene networks can produce morphological structures that are usually considered to be homologs, and non-homologous structures can express homologous genes.
Developmental biologists therefore often prefer a process-oriented concept of homology, which they call 'biological homology', where homologous features are those sharing a set of developmental constraints (Wagner 1989). Indeed, the terms 'syngeny' (Butler and Saidel 2000) and 'homocracy' (Nielsen and Martinez 2003) have been coined to describe morphological features that are organized through the expression of homologous gene networks, irrespective of whether those features are evolutionarily homologous or convergent.
Reticulation and homology
This idea can be extended to other evolutionary scenarios. The one I am particularly interested in here is the consequence of reticulation. In the situations discussed above the character modifications (ancestral to derived) come from "within" the lineage (traditional ancestor-descendant gene inheritance), but the modifications can also come from "outside", by gene flow.
For example, Andam and Gogarten (2012) have noted that horizontal gene transfer (HGT) can in fact be used to provide information for the concept of a Tree of Life, because a transferred gene can also be regarded as a shared derived character. That is, HGT of a gene into an ancestor forms a synapomorphy for its descendants. This gene may subsequently diversify among those descendants, even following a simple tree-like pattern of descent.
This creates a terminological issue. If diversification occurs, then these genes are homologous in the traditional sense (they are modified descendants of a common ancestral character). However, how do they compare to genes in the descendants of species that did not receive the HGT, and to the genes from which the transfer occurred? In the first case they are not applicable (just as the concept of wings is not applicable to animals with flippers). In the second case our current concept of homology does not apply in any simple sense.
The hierarchical concept of homology is tied to a tree model of evolution. The hierarchical nature of characters results from the nested hierarchy of taxon relationships. If there is no nested hierarchy of taxon relationships then our current concepts of homology are inadequate. We need terms that describe possible reticulate relationships among the characters, not just hierarchical ones.
Thus, along with modifications to the concept of monophyly (see Monophyletic groups in networks ), networks imply that we need modifications to the concept of homology, as well.
It is worth noting that a similar issue applies in other fields that are based on a concept of evolutionary history. For example, in historical linguistics words are considered to descend from ancestral languages and diversify among multiple daughter languages. These words are considered to be cognate (cf. homologous). However, words are also borrowed from unrelated languages, and these are loan words (cf. HGT). Loan words may also diversify among the daughter languages, both in the original language and in the borrowing language.
For example, the Germanic word *rīks (ruler) was borrowed from Celtic *rīxs (king), and it has come down to modern times as German 'Reich', English 'rich' (West Germanic), Swedish 'rike' (North Germanic), and Gothic 'reiks' (East Germanic) (see Wikipedia). This diversification has followed Grimm's Law, a regular phonological change that defines the Germanic family — so, the subsequent development of the loan word allows reconstruction of the evolutionary history, and the descendants are cognate. But are they cognate to the words descended from *rīxs within Celtic?
Andam CP, Gogarten JP (2013) Biased gene transfer contributes to maintaining the Tree of Life. In: Lateral Gene Transfer in Evolution (U Gophna, ed.), pp 263-274. Springer: New York.
Butler AB, Saidel WM (2000) Defining sameness: historical, biological, and generative homology. Bioessays 22: 846-853.
Fitch WM (2000) Homology: a personal view on some of the problems. Trends in Genetics 16: 227-231.
Meyer A (1999) Homology and homoplasy: the retention of genetic programmes. In: Homology (GR Bock, G Cardew, eds), pp. 141-157. Wiley: Chichester.
Mindell DP, Meyer A (2001) Homology evolving. Trends in Ecology and Evolution 16: 434-440.
Nielsen C, Martinez P (2003) Patterns of gene expression: homology or homocracy? Development Genes and Evolution 213: 149-154.
Wagner GP (1989) The biological homology concept. Annual Review of Ecology and Systematics 20: 51-69.
Wagner GP (2014) Homology, Genes, and Evolutionary Innovation. Princeton University Press: Princeton NJ.