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.     

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.     

Comparative genomics and evolutionary biology

Data of large-scale DNA sequencing are relevant to some of the most fundamental issues in evolutionary biology: suboptimality, homology, hierarchy, ancestry, novelties, the role of natural selection, and the relative importance of directional versus stabilizing selection. Already, these data provided the best available evidence for some evolutionary phenomena, and in several cases led to refinement of old concepts. Still, the Darwinian evolutionary paradigm will successfully accommodate comparative genomics.     

Field homology: a meaningless concept.

Most biological homologues involve comparison of single characters in two or more taxa. It is possible, however, to recognize homologous characters between two or more taxa that involve the transformation of one character into many characters or many characters into one character. This type of homology is recognized as field homology and it has been widely used in comparative neuroanatomy. The emergence of the cladistic analysis of embryonic stages in the development of neural characters, however, strongly suggests that field homology is a meaningless concept. When it appears necessary to recognize field homologues, it is because comparisons are being made at an inappropriate level within a given biological hierarchy. Furthermore, recognition of field homologues restricts evolutionary mechanisms to a single mechanism of parcellation as defined by Ebbesson.     

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.     

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.     

Homology: Why We Know a Whale Is Not a Fish

Homology is a fundamental concept in comparative and evolutionary biology and yet often the focus of antievolution challenges. In describing structural similarity that is the result of common ancestry, hypotheses about homology require rigorous testing and form the basis for making predictions about anatomy and physiology as well as the fossil record. Communicating the basics of homology to students is essential for a high school biology curriculum.     

Units and passages: A view for evolutionary biology and ecology

Many authors, including paleobiologists, cladists and so on, adopt a nested hierarchical viewpoint to examine the relationships among different levels of biological organization. Furthermore, species are often considered to be unique entities in functioning evolutionary processes and one of the individuals forming a nested hierarchy.I have attempted to show that such a hierarchical view is inadequate in evolutionary biology. We should define units depending on what we are trying to explain. Units that play an important role in evolution and ecology do not necessarily form a nested hierarchy. Also the relationships among genealogies at different levels are not simply nested. I have attempted to distinguish the different characteristics of passages when they are used for different purposes of explanation. In my analysis, species and monophyletic taxa cannot be uniquely defined as single units that function in ecological and evolutionary processes.The view discussed in this paper may provide a more general basis for testing competing theories in evolution, and provide new insights for future empirical studies.     

Homology in Development and the Development of the Homology Concept

Homology is a central concept for Developmental Evolution. HereI argue that homology should be explained within the referenceprocesses of development and evolution; development becauseit is the proximate cause of morphological characters and evolutionbecause it deals with organic transformations and stability.This was already recognized by Hans Spemann in 1915. In a seminalessay "A history and critique of the homology concept" Spemannanalyzed the history and present problems of the homology concept.Here I will continue Spemann's project and analyze some of the20th century contributions to homology. I will end with a fewreflections about the connections between developmental processesand homology and conclude that developmental processes are inherentin (i) the assessment of homology, (ii) the explanation of homology,(iii) the origin of evolutionary innovations (incipient homologues),and (iv) can be considered homologous themselves.     

Levels of biological organization and the origin of novelty

The concept of novelty in evolutionary biology pertains to multiple tiers of biological organization from behavioral and morphological changes to changes at the molecular level. Identifying novel features requires assessments of similarity (homology and homoplasy) of relationships (phylogenetic history) and of shared developmental and genetic pathways or networks. After a brief discussion of how novelty is used in recent literature, we discuss whether the evolutionary approach to homology and homoplasy initially formulated by Lankester in the 19th century informs our understanding of novelty today. We then discuss six examples of morphological features described in the recent literature as novelties, and assess the basis upon which they are regarded as novel. The six are: origin of the turtle shell, transition from fish fins to tetrapod limbs, origination of the neural crest and neural crest cells, cement glands in frogs and casquettes in fish, whale bone-eating tubeworms, and the digestion of plant proteins by nematodes. The article concludes with a discussion of means of acquiring novel genetic information that can account for novelty recognized at higher levels. These are co-options of existing genetic circuitry, gene duplication followed by neofunctionalization, gene rearrangements through mobile genetic elements, and lateral gene transfer. We conclude that on the molecular level only the latter category provides novel genetic information, in that there is no homologous precursor. However, novel phenotypes can be generated through both neofunctionalization and gene rearrangements. Therefore, assigning phenotypic or genotypic "novelty" is contingent on the level of biological organization addressed.     

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.

Do Organisms Exist?

What is the status of organisms in modern evolutionary biology?I argue that this is a question which centers on the questionof reduction, and towards a complete answer, I pursue issuesthrough three different senses of the term: ontological, methodological,and epistemological. The first sense refers to the ultimatestatus of the entities of the organic world, and in this senseI argue that organisms have no special status. The second senserefers to the question of organization, and I argue that inthe light of modern evolutionary biology organisms do have adistinctive "design-like" organization. The third sense refersto the relationship between theories, in particular to whetherthe theories of the biological sciences can be shown to be logicalconsequences of the theories of the physical sciences. I arguethat such reduction may be possible in principle but difficultin practice. However, from the perspective of the working scientist,this hardly matters. In conclusion, I argue that in some respectsorganisms are not distinctive and in other respects they are.Certainly biologists need not worry for the autonomy of theirsubject.     

Unburdening evo-devo: ancestral attractions, model organisms, and basal baloney

Although flourishing, I argue that evo-devo is not yet a mature scientific discipline. Its philosophical foundation exhibits an internal inconsistency that results from a metaphysical confusion. In modern evolutionary biology, species and other taxa are most commonly considered as individuals. I accept this thesis to be the best available foundation for modern evolutionary biology. However, evo-devo is characterized by a remarkable degree of typological thinking, which instead treats taxa as classes. This metaphysical incompatibility causes much distorted thinking. In this paper, I will discuss the logical implications of accepting the individuality thesis for evo-devo. First, I will illustrate the degree to which typological thinking pervades evo-devo. This ranges from the relatively innocent use of typologically tainted language to the more serious misuse of differences between taxa as evidence against homology and monophyly, and the logically flawed concept of partial homology. Second, I will illustrate how, in a context of typological thinking, evo-devo's harmless preoccupation with distant ancestors has become transformed into a pernicious problem afflicting the choice of model organisms. I will expose the logical flaws underlying the common assumption that model organisms can be expected to represent the clades they are a part of in an unambiguous way. I will expose the logical flaws underlying the general assumption that basal taxa are the best available stand-ins for ancestors and that they best represent the clade of which they are a part, while also allowing for optimal extrapolation of results.     

The cell theory--history, present state and prospects (on the 150th anniversary of the development of the cell theory)

The main stages of history of this most important biological conception are presented and the state of the modern cell theory and its future prospects are considered. Since 1839, when T. Schwann expounded his conception of the cell, a long pathway in cognition of the cell function and organization has been covered. From the original picture of the complex organism as a "cellular state", made up of relatively independent "elementary organisms", i.e. cells the modern biology has come to the idea of the cell as an integral system either being a part of a complex organism, or living free in the nature (protists). The cell represents certain qualitatively peculiar level in a complex evolutionary established hierarchy of biological systems. Some particular tight relations, existing between cytology, as a fundamental biological science and molecular biology, genetics, ecology and other biological disciplines are considered. The importance of the cell conception is ascertained for practical aims, especially in medicine.     

Reviving the superorganism

Individuals become functionally organized to survive and reproduce in their environments by the process of natural selection. The question of whether larger units such as groups and communities can possess similar properties of functional organization, and therefore be regarded as "superorganisms", has a long history in biological thought. Modern evolutionary biology has rejected the concept of superorganisms, explaining virtually all adaptations at the individual or gene level. We criticize the modern literature on three counts. First, individual selection in its strong form is founded on a logical contradiction, in which genes-in-individuals are treated differently than individuals-in-groups or species-in-communities. Imposing consistency clearly shows that groups and communities can be organisms in the same sense that individuals are. Furthermore, superorganisms are more than just a theoretical possibility and actually exist in nature. Second, the view that genes are the "ultimate" unit of selection is irrelevant to the question of functional organization. Third, modern evolutionary biology includes numerous conceptual frameworks for analyzing evolution in structured populations. These frameworks should be regarded as different ways of analyzing a common process which, to be correct, must converge on the same conclusions. Unfortunately, evolutionists frequently regard them as competing theories that invoke different mechanisms, such that if one is "right" the others must be "wrong". The problem of multiple frameworks is aggravated by the fact that major terms, such as "units of selection", are defined differently within each framework, yet many evolutionists who use one framework to argue against another assume shared meanings. We suggest that focusing on the concept of organism will help dispell this fog of semantic confusion, allowing all frameworks to converge on the same conclusions regarding units of functional organization.     

TRIBUTE: In Goethe's Wake: Marvalee Wake's conceptual contributions to the development and evolution of a science of morphology

Decrying the typological approach in much of the teaching of morphology, from the outset of her career Marvalee Wake advocated a synthetic, mechanistic and pluralistic developmental and evolutionary morphology. In this short essay, I do not evaluate Wake's contributions to our knowledge of the morphology of caecilians, nor her contributions to viviparity, both of which are seminal and substantive, nor do I examine her role as mentor, supervisor and collaborator, but assess her broader conceptual contributions to the development and evolution of morphology as a science. One of the earliest morphologists to take on board the concept of constraint, she viewed constraint explicitly in relation to adaptation and diversity. Her approach to morphology as a science was hierarchical – measure form and function in a phylogenetic context; seek explanations at developmental, functional, ecological, evolutionary levels of the biological hierarchy; integrate those explanations to the other levels. The explanatory power of morphology thus practised allows morphology to inform evolutionary biology and evolutionary theory, and paves the way for the integrative biology Wake has long championed.     

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.     

Branches in the lines of descent: Charles Darwin and the evolution of the species concept

Charles Darwin introduced a novel idea into the concept of species, namely that species are branches in the lines of descent (segments of population lineages). In addition to this novel evolutionary component, Darwin's species concept also retained an older taxonomic component, namely the view that the species category is a taxonomic rank; moreover, he adopted amount of difference as a criterion for ranking lineages as species. Subsequent biologists retained both components of Darwin's species concept, although they replaced Darwin's ranking criterion with ranking criteria that either are more objectively defined or relate more directly to the biological bases of lineage separation and divergence. Numerous alternative ranking criteria were proposed, resulting in a proliferation of species definitions and a controversy concerning the concept of species. That controversy can be resolved by distinguishing more explicitly between the theoretical concept of species and the operational criteria that are used to apply the concept in practice. By viewing the various alternative ranking criteria as operational indicators of lineage separation rather than necessary properties of species, the conflicts among competing species concepts are eliminated, resulting in a unified concept of species. A brief examination of the history of biology reveals that an important shift related to the unified species concept has been emerging ever since Darwin reformulated the concept of species with an evolutionary basis. The species category is effectively being decoupled from the hierarchy of taxonomic ranks and transferred to the hierarchy of biological organization. Published 2011. This article is a US Government work and is in the public domain in the USA. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 19–35.     

Function without purpose

Philosophers of evolutionary biology favor the so-called etiological concept of function according to which the function of a trait is its evolutionary purpose, defined as the effect for which that trait was favored by natural selection. We term this the selected effect (SE) analysis of function. An alternative account of function was introduced by Robert Cummins in a non-evolutionary and non-purposive context. Cummins's account has received attention but little support from philosophers of biology. This paper will show that a similar non-purposive concept of function, which we term causal role (CR) function, is crucial to certain research programs in evolutionary biology, and that philosophical criticisms of Cummins's concept are ineffective in this scientific context. Specifically, we demonstrate that CR functions are a vital and ineliminable part of research in comparative and functional anatomy, and that biological categories used by anatomists are not defined by the application of SE functional analysis. Causal role functions are non-historically defined, but may themselves be used in an historical analysis. Furthermore, we show that a philosophical insistence on the primary of SE functions places practicing biologists in an untenable position, as such functions can rarely be demonstrated (in contrast to CR functions). Biologists who study the form and function of organismal design recognize that it is virtually impossible to identify the past action of selection on any particular structure retrospectively, a requirement for recognizing SE functions.