When is homology not homology?

Although genes have specific phenotypic consequences in a given species, this functional relationship can clearly change during the course of evolution. Many cases of evolutionary dissociations between homologous genes and homologous morphological features are now known. These dissociations have interesting and important implications for understanding the genetic basis for evolutionary change in morphology.     

On homology

Homology in cladistics is reviewed. The definition of important terms is explicated in historical context. Homology is not synonymous with synapomorphy: it includes symplesiomorphy, and Hennig clearly included both plesiomorphy and synapomorphy as types of homology. Homoplasy is error, in coding, and is analogous to residual error in simple regression. If parallelism and convergence are to be distinguished, homoplasy would be evidence of the former and analogy evidence of the latter. We discuss whether there is a difference between molecular homology and morphological homology, character state homology, nested homology (additive characters), and serial homology. We conclude by proposing a global definition of homology. ©The Will Henning Society 2011.     

On homology

The currently most widely used definitions of homology, which concentrate exclusively on what I call phylogenetic homology, involve comparisons between taxa. Although they share important conceptual relationships with phylogenetic homology and their role in evolutionary biology is significant, serial and other forms of iterative homology have been, by comparison, overlooked. There is need for a more inclusive definition of homology. I propose that the basis of homology in the broad sense is the sharing of pathways of development, which are controlled by genealogically-related genes. Using this definition, one can construct hierarchies of homology, and recognize different degrees or strengths of homology. Because different aspects of structures are controlled by distinct developmental programs, it is sometimes necessary to speak of homologies of different attributes of specific structures, rather than to homologize the structures per se. For good biological reasons, parallelism may be difficult to distinguish from homology, and one must in practice be willing to tolerate some ambiguity between them. The formulation I present leads to some unorthodox conclusions about homology in mammalian dentitions and homology between the fore-and hindlimbs of tetrapods.     

Ancestors and homology

Current issues concerning the nature of ancestry and homology are discussed with reference to the evolutionary origin of the tetrapod limb. Homologies are argued to be complex conjectural inferences dependant upon a pre-existing phylogenetic analysisand a theoretical model of the evolutionary development of ontogenetic information. Ancestral conditions are inferred primarily from character (synapomorphy/homology) distributions within phylogeny, because of the deficiencies of palaeontological data. Recent analyses of tetrapod limb ontogeny, and the diverse, earliest morphologies known from the fossil record, are inconsistent with typological concepts such as fixed ancestral patterns or bauplans, emphasising the incompatibility of these with evolutionary continuity. The evolutionary origin of the tetrapod limb is also examined in the light of its recent discussion in developmental genetics. While this field promises to reveal more of the fundamental ontogenetic content of homology (identity), at present it is concerned mostly with the abstraction of a new set of types, rather than investigating diversity and change.     

Functional homology and homology of function: biological concepts and philosophical consequences

“Functional homology” appears regularly in different areas of biological research and yet it is apparently a contradiction in terms—homology concerns identity of structure regardless of form and function. I argue that despite this conceptual tension there is a legitimate conception of ‘homology of function’, which can be recovered by utilizing a distinction from pre-Darwinian physiology (use versus activity) to identify an appropriate meaning of ‘function’. This account is directly applicable to molecular developmental biology and shares a connection to the theme of hierarchy in homology. I situate ‘homology of function’ within existing definitions and criteria for structural assessments of homology, and introduce a criterion of ‘organization’ for judging function homologues, which focuses on hierarchically interconnected interdependencies (similar to relative position and connection for skeletal elements in structural homology). This analysis of biological concepts has at least three broad philosophical consequences: (1) it provides the grounds for the study of behavior and psychological categories as homologues; (2) it demonstrates that philosophers who take selected effect function as primary effectively ignore large portions of comparative, structural, and experimental research, thereby misconstruing biological reasoning and knowledge; and, (3) it underwrites causal generalizations, which illuminates inferences made from model organisms in experimental biology.

Good characters and homology

This paper is a critical comment on a recent article by Lieberman. 1 We question his opinion that DNA is a better data source for phylogenetic reconstructions than bone and discuss his “problems and potential solutions” regarding the homology concept. We conclude that phylogenetic systematics requires a phylogenetic homology concept, and that Lieberman's “solutions,” though useful terms, should not be designated as homology.     

Using multiple templates to improve quality of homology models in automated homology modeling

When researchers build high-quality models of protein structure from sequence homology, it is today common to use several alternative target-template alignments. Several methods can, at least in theory, utilize information from multiple templates, and many examples of improved model quality have been reported. However, to our knowledge, thus far no study has shown that automatic inclusion of multiple alignments is guaranteed to improve models without artifacts. Here, we have carried out a systematic investigation of the potential of multiple templates to improving homology model quality. We have used test sets consisting of targets from both recent CASP experiments and a larger reference set. In addition to Modeller and Nest, a new method (Pfrag) for multiple template-based modeling is used, based on the segment-matching algorithm from Levitt's SegMod program. Our results show that all programs can produce multi-template models better than any of the single-template models, but a large part of the improvement is simply due to extension of the models. Most of the remaining improved cases were produced by Modeller. The most important factor is the existence of high-quality single-sequence input alignments. Because of the existence of models that are worse than any of the top single-template models, the average model quality does not improve significantly. However, by ranking models with a model quality assessment program such as ProQ, the average quality is improved by approximately 5% in the CASP7 test set.     

Quantitative tests of primary homology

In systematic biology homology hypotheses are typically based on points of similarity and tested using congruence, of which the two stages have come to be distinguished as “primary” versus “secondary” homology. Primary homology is often regarded as prior to logical test, being a kind of background assumption or prior knowledge. Similarity can, however, be tested by more detailed studies that corroborate or weaken previous homology hypotheses before the test of congruence is applied. Indeed testing similarity is the only way to test the homology of characters, as congruence only tests their states. Traditional homology criteria include topology, special similarity, function, ontogeny and step‐counting (for example, transformation in one step versus two via loss and gain). Here we present a method to compare quantitatively the ability of such criteria, and competing homology schema, to explain morphological observations. We apply the method to a classic and difficult problem in the homology of male spider genital sclerites. For this test case topology performed better than special similarity or function. Primary homologies founded on topology resulted in hypotheses that were globally more parsimonious than those based on other criteria, and therefore yielded a more coherent and congruent nomenclature of palpal sclerites in theridiid spiders than prior attempts. Finally, we question whether primary homology should be insulated as “prior knowledge” from the usual issues and demands that quantitative phylogenetic analyses pose, such as weighting and global versus local optima. © The Willi Hennig Society 2007.     

Developmental genetics and traditional homology

The concept of homology arose from classical studies of comprative morphology, and took on a new signficance with the advent of evolutionary theory. It is currentlyl undergoing antoher metamorphosis: many developmental geneticists now dfine homology as shared patterns of gene expression. However, this ne usage conflaes difinition with criteri, and fails to recognize the meaninful asignments of homology must speify a biologcal level. We argue the although developmental genetic data can help identify homologus structures. they are niether necessary nor sufficient, and do not in any case jutify a new definition of homology.     

Parallelism and non-parallelism in homology

Acta Biotheoretica -