Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept

The present paper analyzes the use and understanding of the homology concept across different biological disciplines. It is argued that in its history, the homology concept underwent a sort of adaptive radiation. Once it migrated from comparative anatomy into new biological fields, the homology concept changed in accordance with the theoretical aims and interests of these disciplines. The paper gives a case study of the theoretical role that homology plays in comparative and evolutionary biology, in molecular biology, and in evolutionary developmental biology. It is shown that the concept or variant of homology preferred by a particular biological field is used to bring about items of biological knowledge that are characteristic for this field. A particular branch of biology uses its homology concept to pursue its specific theoretical goals.     

The types of homology and their significance for evolutionary biology and phylogenetics

This paper comments on recently revived discussion about the most adequate definition of homology. Homologues are considered as similarities of complex structures or patterns which are based on a continuity of biological information or instruction. Dependent on the level of comparison four types of homology are defined: (1) Iterative ( = serial = homonomy), (2) ontogenetic, (3) di- or polymorphic, and (4) supraspecific homology. The significance of all four types for evolutionary biology and phylogenetic analysis is outlined.     

形态性状、分子性状与同源性

“同源性(homology)”是生物学中最基本的概念之一。近年来, 随着分子生物学、生物信息学、发育生物学以及进化发育遗传学等学科的快速发展, 同源性一词在形态性状的比较、核苷酸和氨基酸序列的分析以及探讨形态性状进化的分子机制等方面都有广泛应用。然而, 由于不同的研究者对同源性概念的理解有所不同, 在实际应用中难免会出现不恰当使用“同源性”一词并得出错误结论的情况。本文从不同的角度介绍了如何对同源性进行判断以及影响同源性判断的因素。并指出正确理解同源性这一概念的含义, 以及通过综合各方面的证据对同源性进行推断对于揭示基因型和表型的进化以及二者之间的关系非常重要。     

形态性状、分子性状与同源性

“同源性（homology）”是生物学中最基本的概念之一。近年来,随着分子生物学、生物信息学、发育生物学以及进化发育遗传学等学科的快速发展,同源性一词在形态性状的比较、核苷酸和氨基酸序列的分析以及探讨形态性状进化的分子机制等方面都有广泛应用。然而,由于不同的研究者对同源性概念的理解有所不同,在实际应用中难免会出现不恰当使用“同源性”一词并得出错误结论的情况。本文从不同的角度介绍了如何对同源性进行判断以及影响同源性判断的因素。并指出正确理解同源性这一概念的含义,以及通过综合各方面的证据对同源性进行推断对于揭示基因型和表型的进化以及二者之间的关系非常重要。     

Phylogeny and evo-devo: characters, homology, and the historical analysis of the evolution of development

The concept of homology continues to attract more and more commentary. In systematic and evolutionary biology the meaning of homology as synapomorphic similarity inherited from a common ancestor has gained wide acceptance over the last three or four decades. In recent years, however, developmental biologists, in particular, have argued for a new approach to, and new definition for, homology that revolves around the desire to make it more process-oriented and more mechanistic. These efforts raise questions about the relationship between developmental and evolutionary biology as well as how the evolution of development is to be studied. It is argued in this paper that this new approach to homology seemingly decouples developmental biology from the study of the evolution of development rather than to facilitate that study. In contrast, applying the notion of historical, phylogenetic homology to developmental data is inherently comparative and therefore evolutionary.     

Evo-devo and the search for homology (“sameness”) in biological systems

Developmental biology and evolutionary studies have merged into evolutionary developmental biology (“evo-devo”). This synthesis already influenced and still continues to change the conceptual framework of structural biology. One of the cornerstones of structural biology is the concept of homology. But the search for homology (“sameness”) of biological structures depends on our favourite perspectives (axioms, paradigms). Five levels of homology (“sameness”) can be identified in the literature, although they overlap to some degree: (i) serial homology (homonomy) within modular organisms, (ii) historical homology (synapomorphy), which is taken as the only acceptable homology by many biologists, (iii) underlying homology (i.e., parallelism) in closely related taxa, (iv) deep evolutionary homology due to the “same” master genes in distantly related phyla, and (v) molecular homology exclusively at gene level. The following essay gives emphasis on the heuristic advantages of seemingly opposing perspectives in structural biology, with examples mainly from comparative plant morphology. The organization of the plant body in the majority of angiosperms led to the recognition of the classical root–shoot model. In some lineages bauplan rules were transcended during evolution and development. This resulted in morphological misfits such as the Podostemaceae, peculiar eudicots adapted to submerged river rocks. Their transformed “roots” and “shoots” fit only to a limited degree into the classical model which is based on either–or thinking. It has to be widened into a continuum model by taking over elements of fuzzy logic and fractal geometry to accommodate for lineages such as the Podostemaceae.     

Assessing similarity: on homology,characters and the need for a semantic approach to non‐evolutionary comparative homology

The problem of homology has been a consistent source of controversy at the heart of systematic biology, as has the step of morphological character analysis in phylogenetics. Based on a clear epistemic framework and a characterization of “characters” as diagnostic evidence units for the recognition of not directly identifiable entities, I discuss the ontological definition and empirical recognition criteria of phylogenetic, developmental and comparative homology, and how these three accounts of homology each contribute to an understanding of the overall phenomenon of homology. I argue that phylogenetic homologies are individuals or historical kinds that require comparative homology for identification. Developmental homologies are natural kinds that ultimately rest on phylogenetic homologies and also require comparative homology for identification. Comparative homologies on the other hand are anatomical structural kinds that are directly identifiable. I discuss pre‐Darwinian comparative homology concepts and their problem of invoking non‐material forces and involving the a priori assumption of a stable positional reference system. Based on Young's concept of comparative homology, I suggest a procedure for recognizing comparative homologues that lacks these problems and that utilizes a semantic framework. This formal conceptual framework provides the much needed semantic transparency and computer‐parsability for documenting, communicating and analysing similarity propositions. It provides an essential methodological framework for generalizing over individual organisms and identifying and demarcating anatomical structural kinds, and it provides the missing link to the logical chain of identifying phylogenetic homology. The approach substantially increases the analytical accessibility of comparative research and thus represents an important contribution to the theoretical and methodological foundation of morphology and comparative biology.     

CONCEPTS AND TESTS OF HOMOLOGY IN THE CLADISTIC PARADIGM

Abstract— Logical equivalence between the notions of homology and synapomorphy is reviewed and supported. So-called transformational homology embodies two distinct logical components, one related to comparisons among different organisms and the other restricted to comparisons within the same organism. The former is essentially hierarchical in nature, thus being in fact a less obvious form of taxic homology. The latter is logically equivalent to so-called serial homology in a broad sense (including homonomy, mass homology or iterative homology). Of three tests of homology proposed to date (similarity, conjunction and congruence) only congruence serves as a test in the strict sense. Similarity stands at a basic level in homology propositions, being the source of the homology conjecture in the first place. Conjunction is unquestionably an indicator of non-homology, but it is not specific about the pairwise comparison where non-homology is present, and depends on a specific scheme of relationship in order to refute a hypothesis of homology. The congruence test has been previously seen as an application of compatibility analysis. However, congruence is more appropriately seen as an expression of strict parsimony analysis. A general theoretical solution is proposed to determine evolution of characters with ambiguous distributions, based on the notion of maximization of homology propositions. According to that notion, ambiguous character-state distributions should be resolved by an optimization that maximizes reversals relative to parallelisms. Notions of homology in morphology and molecular biology are essentially the same. The present tendency to adopt different terminologies for the two sources of data should be avoided, in order not to obscure the fundamental uniformity of the concept of homology in comparative biology. “A similar hierarchy is found both in ‘structures’ and in ‘functions’. In the last resort, structure (i.e. order of parts) and function (order of processes) may be the very same thing […].” L. von Bertalanlfy “[…] it is the fact that certain criteria enable us to match parts of things consistently which suggests that mechanisms of certain kinds must have been involved in their origin.” N. Jardine and C. Jardine     

Homology in classical and molecular biology

Hypotheses of homology are the basis of comparative morphology and comparative molecular biology. The kinds of homologous and nonhomologous relations in classical and molecular biology are explored through the three tests that may be applied to a hypothesis of homology: congruence, conjunction, and similarity. The same three tests apply in molecular comparisons and in morphology, and in each field they differentiate eight kinds of relation. These various relations are discussed and compared. The unit or standard of comparison differs in morphology and in molecular biology; in morphology it is the adult or life cycle, but with molecules it is the haploid genome. In morphology the congruence test is decisive in separating homology and nonhomology, whereas with molecular sequence data similarity is the decisive test. Consequences of this difference are that the boundary between homology and nonhomology is not the same in molecular biology as in morphology, that homology and synapomorphy can be equated in morphology but not in all molecular comparisons, and that there is no detected molecular equivalent of convergence. Since molecular homology may reflect either species phylogeny or gene phylogeny, there are more kinds of homologous relation between molecular sequences than in morphology. The terms paraxenology and plerology are proposed for two of these kinds--respectively, the consequence of multiple xenology and of gene conversion.     

Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899-1972)

The evolutionary embryologist Gavin Rylands de Beer can be viewed as one of the forerunners of modern evolutionary developmental biology in that he posed crucial questions and proposed relevant answers about the causal relationship between ontogeny and phylogeny. In his developmental approach to the phylogenetic phenomenon of homology, he emphasized that homology of morphological structures is to be identified neither with the sameness of the underlying developmental processes nor with the homology of the genes that are involved in the development of the structures. De Beer's work on developmental evolution focused on the notion of heterochrony, arguing that paedomorphosis increases morphological evolvability and is thereby an important mode of evolution that accounts for the origin of many taxa, including higher taxa.     

Homology and the hierarchy of biological systems

Homology is the similarity between organisms due to common ancestry. Introduced by Richard Owen in 1843 in a paper entitled "Lectures on comparative anatomy and physiology of the invertebrate animals", the concept of homology predates Darwin's "Origin of Species" and has been very influential throughout the history of evolutionary biology. Although homology is the central concept of all comparative biology and provides a logical basis for it, the definition of the term and the criteria of its application remain controversial. Here, I will discuss homology in the context of the hierarchy of biological organization. I will provide insights gained from an exemplary case study in evolutionary developmental biology that indicates the uncoupling of homology at different levels of biological organization. I argue that continuity and hierarchy are separate but equally important issues of homology.     

Contemporary concepts of homology in biology (a theoretical review)

A brief review of the contemporary theoretical concepts of homology being developed basically in systematics and phylogenetics as well as in developmental biology is presented. Ontologically, both homology and analogy represent a kind of correspondence considered from the standpoint of nominalism, realism, and conceptualism. According to their nominalistic treatment, both are described by a set-theory approximation which makes them classes (in the logical sense). The realistic treatment provides their holistic view according to which a homologue is an anatomical or evolutionary singular while analogue remains a class. The conceptualistic treatment means that there are real (objective) correspondences existing among real (objective) entities while fixation of any of them is based on certain theoretical presumptions adopted by a researcher; homology as a natural kind (including homeostatic property cluster) seems to be most consistent with such a treatment. Realistic view of homology makes it "absolute", while two others make discrimination of homology and analogy strictly relative. Two basic general homology concepts have been developed in recent literature--taxic and transformational ones; the first considers respective correspondences as structure relations, the second as process relations. The taxic homology is nearly the same as classical typological one (Owen), while transformational homology unites all its phylogenetic, ontogenetic (developmental) and transformation-typological definitions. Process-structuralistic approach seems to unite both taxic and transformational ones. The latter makes it possible to apply general homology concept not only to structures but to processes as well. It is stressed that homology is not identical to the similarity, the latter being just the means for revealing the former. Some closer consideration is given to phylogenetic, ontogenetic and genetic treatments of homology; significant uncertainty is shown to exist between them which causes the "homology problem". Epistemologically, any homology statement has a status of hypothesis which makes such a statement theory-dependent according to the hypothetic-deductive argumentation scheme. This dependence allows to stress once more the relative nature of homology and analogy correspondences. Some questions concerning operational concepts and criteria of homology are considered. A hierarchical concept of homology seems to be the most promising prospect of future development of the "homology problem".     

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.     

Perspective: the origin of flowering plants and their reproductive biology--a tale of two phylogenies

Recently, two areas of plant phylogeny have developed in ways that could not have been anticipated, even a few years ago. Among extant seed plants, new phylogenetic hypotheses suggest that Gnetales, a group of nonflowering seed plants widely hypothesized to be the closest extant relatives of angiosperms, may be less closely related to angiosperms than was believed. In addition, recent phylogenetic analyses of angiosperms have, for the first time, clearly identified the earliest lineages of flowering plants: Amborella, Nymphaeales, and a clade that includes Illiciales/ Trimeniaceae/Austrobaileyaceae. Together, the new seed plant and angiosperm phylogenetic hypotheses have major implications for interpretation of homology and character evolution associated with the origin and early history of flowering plants. As an example of the complex and often unpredictable interplay of phylogenetic and comparative biology, we analyze the evolution of double fertilization, a process that forms a diploid embryo and a triploid endosperm, the embryo-nourishing tissue unique to flowering plants. We demonstrate how the new phylogenetic hypotheses for seed plants and angiosperms can significantly alter previous interpretations of evolutionary homology and firmly entrenched assumptions about what is synapomorphic of flowering plants. In the case of endosperm, a solution to the century-old question of its potential homology with an embryo or a female gametophyte (the haploid egg-producing generation within the life cycle of a seed plant) remains complex and elusive. Too little is known of the comparative reproductive biology of extant nonflowering seed plants (Gnetales, conifers, cycads, and Ginkgo) to analyze definitively the potential homology of endosperm with antecedent structures. Remarkably, the new angiosperm phylogenies reveal that a second fertilization event to yield a biparental endosperm, long assumed to be an important synapomorphy of flowering plants, cannot be conclusively resolved as ancestral for flowering plants. Although substantive progress has been made in the analysis of phylogenetic relationships of seed plants and angiosperms, these efforts have not been matched by comparable levels of activity in comparative biology. The consequence of inadequate comparative biological information in an age of phylogenetic biology is a severe limitation on the potential to reconstruct key evolutionary historical events.     

Phenotypic Integration Patterns Support an Account of Homology as a Manifestation of Evolvability

Data gleaned from the study of phenotypic integration provide important empirical support for a recent theoretical advance in evolutionary developmental biology, in which the phenomenon of homology is construed as an aspect of evolvability. The presence of highly conserved phenotypic covariation structure among distantly related taxa suggests the action of developmental processes that allow the generation of variation while maintaining stability and functionality.     

The Formation of the Theory of Homology in Biological Sciences

Homology is among the most important comparative concepts in biology. Today, the evolutionary reinterpretation of homology is usually conceived of as the most important event in the development of the concept. This paradigmatic turning point, however important for the historical explanation of life, is not of crucial importance for the development of the concept of homology itself. In the broadest sense, homology can be understood as sameness in reference to the universal guarantor so that in this sense the different concepts of homology show a certain kind of "metahomology". This holds in the old morphological conception, as well as in the evolutionary usage of homology. Depending on what is (or was) taken as a guarantor, different types of homology may be distinguished (as idealistic, historical, developmental etc.). This study represents a historical overview of the development of the homology concept followed by some clues on how to navigate the pluralistic terminology of modern approaches to homology.     

Ontogeny, anatomy, and the problem of homology: Carl Gegenbaur and the American tradition of cell lineage studies

Summary In this paper we analyze Carl Gegenbaur’s conception of the relationship between embryology (“Ontogenie”) and comparative anatomy and his related ideas about homology. We argue that Gegenbaur’s conviction of the primacy of comparative anatomy and his careful consideration of caenogenesis led him to a more balanced view about the relationship between ontogeny and phylogeny than his good friend Ernst Haeckel. We also argue that Gegenbaur’s ideas about the centrality of comparative anatomy and his definitions of homology actually laid the conceptual foundations for Hans Spemann’s (1915) later analysis of homology. We also analyze Gegenbaur’s reception in the United States and how the discussions between E.B. Wilson and Edwin Conklin about the role of the “embryological criterion of homology” and the latter’s argument for an even earlier concept of cellular homology reflect the recurring theme of preformism in ontogeny, a theme that finds its modern equivalent in various genetic definitions of homology, only recently challenged by the emerging synthesis of evolutionary developmental biology. Finally, we conclude that Gegenbaur’s own careful methodological principles can serve as an important model for proponents of present day “evo-devo”, especially with respect to the integration of ontogeny with phylogeny embedded in comparative anatomy.     

Bioinformatics and type II G-protein-coupled receptors

The best known family B, or Type II, G-protein-coupled receptors (GPCRs) recognize peptides as ligands. The receptors for corticotrophin-releasing factor, parathyroid hormone and secretin typify this group. However, there are only 15 such GPCRs. Many other receptors share sequence homology and have been assigned to this family. The ten 'Frizzled' and one 'Smoothened' receptors show the lowest sequence homology and are not necessarily G-protein coupled. Drosophila genetics have enabled our understanding of their biology. In contrast, relatively little is known about the largest group with family B, the 33 'large amino termini' or large N-terminal family B seven-transmembrane (LNB 7TM) receptors. This review highlights the similarities found between family B receptors and provides a classification of LNB 7TM receptors.     

羊驼催乳素基因cDNA克隆及序列分析

实验通过克隆分析羊驼催乳素基因的部分序列,对羊驼催乳素基因的结构和功能进行初步探索和揭示。从GeneBank中已报到的脊椎动物催乳素基因保守区设计一对引物,采用Trizol法提取羊驼胎盘总RNA,利用RT-PCR技术扩增出长度约为510 bp的片断。测序后在NCB I工作平台中进行BLASTn同源性比较,得出结论:羊驼催乳素基因与已登录的哺乳动物催乳素基因同源性均超过85%,最高达97%。借助DNAstar分子生物学分析软件绘制了相关动物的遗传进化图,并对羊驼的种属地位进行了进一步验证。。     

Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncogene.

Here we demonstrate that open reading frame 16 (ORF16) of the oncogenic herpesvirus saimiri protects cells from heterologous virus-induced apoptosis. The BH1 and BH2 homology domains are highly conserved in ORF16, and ORF16 heterodimerizes with Bcl-2 family members Bax and Bak. However, ORF16 lacks the core sequence of the conserved BH3 homology domain, suggesting that this region is not essential for anti-apoptotic activity. Conservation of a functional bcl-2 homolog among gammaherpesviruses suggests that inhibition of programmed cell death is important in the biology of these viruses.