Using genetic networks and homology to understand the evolution of phenotypic traits

Homology can have different meanings for different kinds of biologists. A phylogenetic view holds that homology, defined by common ancestry, is rigorously identified through phylogenetic analysis. Such homologies are taxic homologies (=synapomorphies). A second interpretation, "biological homology" emphasizes common ancestry through the continuity of genetic information underlying phenotypic traits, and is favored by some developmental geneticists. A third kind of homology, deep homology, was recently defined as "the sharing of the genetic regulatory apparatus used to build morphologically and phylogenetically disparate features." Here we explain the commonality among these three versions of homology. We argue that biological homology, as evidenced by a conserved gene regulatory network giving a trait its "essential identity" (a Character Identity Network or "ChIN") must also be a taxic homology. In cases where a phenotypic trait has been modified over the course of evolution such that homology (taxic) is obscured (e.g. jaws are modified gill arches), a shared underlying ChIN provides evidence of this transformation. Deep homologies, where molecular and cellular components of a phenotypic trait precede the trait itself (are phylogenetically deep relative to the trait), are also taxic homologies, undisguised. Deep homologies inspire particular interest for understanding the evolutionary assembly of phenotypic traits. Mapping these deeply homologous building blocks on a phylogeny reveals the sequential steps leading to the origin of phenotypic novelties. Finally, we discuss how new genomic technologies will revolutionize the comparative genomic study of non-model organisms in a phylogenetic context, necessary to understand the evolution of phenotypic traits.     

Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution

Homology is at the foundation of comparative studies in biology at all levels from genes to phenotypes. Homology is similarity because of common descent and ancestry, homoplasy is similarity arrived at via independent evolution. However, given that there is but one tree of life, all organisms, and therefore all features of organisms, share some degree of relationship and similarity one to another. That sharing may be similarity or even identity of structure and the sharing of a most recent common ancestor--as in the homology of the arms of humans and apes--or it may reflect some (often small) degree of similarity, such as that between the wings of insects and the wings of birds, groups whose shared ancestor lies deep within the evolutionary history of the Metazoa. It may reflect sharing of entire developmental pathways, partial sharing, or divergent pathways. This review compares features classified as homologous with the classes of features normally grouped as homoplastic, the latter being convergence, parallelism, reversals, rudiments, vestiges, and atavisms. On the one hand, developmental mechanisms may be conserved, even when a complete structure does not form (rudiments, vestiges), or when a structure appears only in some individuals (atavisms). On the other hand, different developmental mechanisms can produce similar (homologous) features. Joint examination of nearness of relationship and degree of shared development reveals a continuum within an expanded category of homology, extending from homology --> reversals --> rudiments --> vestiges --> atavisms --> parallelism, with convergence as the only class of homoplasy, an idea that turns out to be surprisingly old. This realignment provides a glimmer of a way to bridge phylogenetic and developmental approaches to homology and homoplasy, a bridge that should provide a key pillar for evolutionary developmental biology (evo-devo). It will not, and in a practical sense cannot, alter how homoplastic features are identified in phylogenetic analyses. But seeing rudiments, reversals, vestiges, atavisms and parallelism as closer to homology than to homoplasy should guide us toward searching for the common elements underlying the formation of the phenotype (what some have called the deep homology of genetic and/or cellular mechanisms), rather than discussing features in terms of shared or independent evolution.     

Distinguishing between convergence and parallelism is central to comparative biology: a reply to Williams and Ebach

The definitions of character similarity, homology, homoplasy, heterology, parallelism and convergence are clarified in the framework of current phylogenetic methodology. They are all associated with definite patterns of character change and can consequently be tested by phylogeny building. Their crucial significance in comparative biology is illustrated using demonstrative examples. © The Willi Hennig Society 2006.     

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.     

Deconstructing morphology

Scholtz, G. 2010. Deconstructing morphology. —Acta Zoologica (Stockholm) 91 : 44–63 Morphology as the science of form is, in particular, related to the overwhelming diversity of animal forms. Due to its long pre‐Darwinian tradition, organismic morphology is partly burdened by ahistorical typological views. On the other hand, the study of organismic form has always implied concepts of transformation, which helped to pave the way for evolutionary theories. This contradictory history and the fact that we need words to describe organismic form lead in many cases to morphological concepts implying a mixture of structural, functional, developmental, ecological, typological, and evolutionary aspects in current morphological approaches. Because these mixed views lead to contradictory and misleading interpretations of animal form, I stress the need to deconstruct morphological concepts at all levels. I propose a morphology that analyses transformation of animal forms strictly at the structural level in combination with genealogical thinking. Function and other biological aspects of form should be considered in an independent second analytical step. A comparative pattern approach, including developmental patterns, of animal structure in an evolutionary framework allows for the analysis of morphological change, in particular, phylogenetic reconstructions, homology assessment, and the recognition of evolutionary independent morphological units.     

Homoplasy and homology: dichotomy or continuum?

Homology is the presence of the same feature in two organisms whose most recent common ancestor also possessed the feature. I discuss the bases on which we can tell that two features being compared share sufficient elements of sameness to allow them to be treated as homologous and therefore to be legitimately compared with one another in a way that informs comparative, evolutionary, and phylogenetic analysis. To do so, I discuss the relationship(s) between homology and homoplasy to conclude that we are dealing neither with a dichotomy between homoplasy as parallelism/convergence and homology as common descent nor with a dichotomy of homoplasy as the interrupted presence of the character in a lineage and homology as the continuous presence of the character. Rather, we are dealing with common descent with varying degrees of modification. Homoplasy and homology are not dichotomies but the extremes of a continuum, reflecting deep or more recent shared ancestry based on shared cellular mechanisms and processes and shared genes and gene pathways and networks. The same genes can be used to initiate the development of homoplastic and homologous structures. Consequently, structures may be lost but their developmental bases retained, providing the potential for homoplasy. It should not be surprising that similar features persist when a feature is present in the nearest common ancestor (homology). Neither should it be surprising to find that different environments or selective pressures can trigger the reappearance of similar features in organisms that do not share a recent common ancestor (homoplasy).     

The hierarchical basis of serial homology and evolutionary novelty

Given the pervasiveness of gene sharing in evolution and the extent of homology across the tree of life, why is everything not homologous with everything else? The continuity and overlapping genetic contributions to diverse traits across lineages seem to imply that no discrete determination of homology is possible. Although some argue that the widespread overlap in parts and processes should be acknowledged as “partial” homology, this threatens a broad base of presumed comparative morphological knowledge accepted by most biologists. Following a long scientific tradition, we advocate a strategy of “theoretical articulation” that introduces further distinctions to existing concepts to produce increased contrastive resolution among the labels used to represent biological phenomena. We pursue this strategy by drawing on successful patterns of reasoning from serial homology at the level of gene sequences to generate an enriched characterization of serial homology as a hierarchical, phylogenetic concept. Specifically, we propose that the concept of serial homology should be applied primarily to repeated but developmentally individualized body parts, such as cell types, differentiated body segments, or epidermal appendages. For these characters, a phylogenetic history can be reconstructed, similar to families of paralogous genes, endowing the notion of serial homology with a hierarchical, phylogenetic interpretation. On this basis, we propose a five-fold theoretical classification that permits a more fine-grained mapping of diverse trait-types. This facilitates answering the question of why everything is not homologous with everything else, as well as how novelty is possible given that any new character possesses evolutionary precursors. We illustrate the fecundity of our account by reference to debates over insect wing serial homologs and vertebrate paired appendages.     

Plasticity and constraints in development and evolution

Morphological similarities between organisms may be due to either homology or homoplasy. Homologous structures arise by common descent from an ancestral form, whereas homoplasious structures are independently derived in the respective lineages. The finding that similar ontogenetic mechanisms underlie the production of the similar structures in both lineages is not sufficient evidence of homology, as such similarities may also be due to parallel evolution. Parallelisms are a class of homoplasy in which the two lineages have come up with the same solution independently using the same ontogenetic mechanism. The other main class of homoplasy, convergence, is superficial similarity in morphological structures in which the underlying ontogenetic mechanisms are distinct. I argue that instances of convergence and parallelism are more common than is generally realized. Convergence suggests flexibility in underlying ontogenetic mechanisms and may be indicative of developmental processes subject to phenotypic plasticity. Parallelisms, on the other hand, may characterize developmental processes subject to constraints. Distinguishing between homology, parallelisms and convergence may clarify broader taxonomic patterns in morphological evolution.     

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.     

A method for molecular phylogeny construction by direct use of nucleotide sequence data

Summary A method for molecular phylogeny construction is newly developed. The method, called the stepwise ancestral sequence method, estimates molecular phylogenetic trees and ancestral sequences simultaneously on the basis of parsimony and sequence homology. For simplicity the emphasis is placed more on parsiomony than on sequence homology in the present study, though both are certainly important. Because parsimony alone will sometimes generate plural candidate trees, the method retains not one but five candidates from which one can then single out the final tree taking other criteria into account.The properties and performance of the method are then examined by simulating an evolving gene along a model phylogenetic tree. The estimated trees are found to lie in a narrow range of the parsimony criteria used in the present study. Thus, other criteria such as biological evidence and likelihood are necessary to single out the correct tree among them, with biological evidence taking precedence over any other criterion. The computer simulation also reveals that the method satisfactorily estimates both tree topology and ancestral sequences, at least for the evolutionary model used in the present study.     

The use of structural reduction in phylogenetic reconstruction of decapods and a phylogenetic hypothesis for 15 genera of Majidae: testing previous larval hypotheses and assumptions

Summary

Using larval data of zoeae from selected genera of majids, we determined tree topologies, levels of homoplasy, and frequencies of reduction under three different assumptions of character argumentation: ordered reduction events, unordered reduction events, and outgroup comparison. Under each assumption we provided a phylogenetic hypothesis for some majid genera and evaluated the assumption that structural reduction can be assumed a priori as a criterion to infer character transformation polarity in phylogenetic reconstruction of decapods. The results indicate that the a priori assumption of “reduction” as the derived condition is not justified because under this assumption, reduction is not always maintained throughout the resulting phylogenetic hypothesis. Furthermore, we also found that this criterion fails to provide the most parsimonious explanation of the data set. Therefore, we reject the use a “reduction=derived” criterion to infer polarity in phylogenetic reconstruction. Phylogenetic analysis using outgroup comparison provided a phylogenetic hypothesis with a better fit and a lower frequency of reduction events. However, we found that statements of homology may be problematic when the number of larval stages in the outgroup differ from those of the ingroup. To overcome this problem, we suggest that, in the absence of evidence for developmental homology, all larval stages should be considered as potential homologues. Using this approach to homology of larval stages, we provide a new phylogenetic hypothesis for 15 genera of majids based on larval morphology. Within Majidae, representative members of Majinae formed a highly nested monophyletic group with the following topology: ((Jacquinotia+Notomithrax) (Leptomithrax+Maja)). In contrast, the Oregoniinae (Hyas+Chionoecetes) formed a basal monophyletic group. Contrary to established ideas for the monophyly of Inachinae, Macrocheira is basal to the Oregoniinae. Other taxa did not form monophyletic groupings based on classical assignment to subfamilies.     

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.     

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.     

Homoplasy, homology, and the perceived special status of behavior in evolution

Evolutionary biologists tend to tread cautiously when considering how behavioral data might be incorporated into phylogenetic analyses, largely because of the preconception that behavior somehow constitutes a "special" set of characters that may be inherently more prone to homoplasy or subject to different selection regimes than those that operate on the morphological or genetic traits traditionally used in phylogenetic reconstruction. In this review, we first consider how the evolution of behavior has been treated historically, paying particular attention to why phylogenetic reconstruction has often failed to include behavioral traits. We then discuss, from a theoretical perspective, what reasons there are--if any--for assuming that behavioral traits should be more prone to homoplasy than other types of traits. In doing so, we review several empirical studies that tackle this issue head-on. Finally, we examine how behavioral features have been used to good effect in phylogenetic reconstruction. Our conclusion is that there seems to be little justification on theoretical grounds for assuming that behavior is in any way "special"--either particularly labile or particularly prone to exhibit high levels of homoplasy. Additionally, in reviewing historical perceptions of behavior and their links to conceptions of homology, we conclude that there is no compelling reason why behavior cannot be homologized or therefore why it should not prove phylogenetically informative. In subsequently considering several factors related to selection that influence the likelihood of homoplasy occurring in any trait system, we also found no clear trend predicting homoplasy disproportionately in behavioral systems. In fact, where studied, the degree of homoplasy seen in behavioral traits is comparable to that seen in other trait systems. Ultimately, there appear to be no grounds for dismissing behavior a priori from the class of phylogenetically informative characters.     

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".     

A plea for ‘genealogical thinking’ in comparative biology – a rebuttal to the reply of Szucsich,Wirkner, and Pass to my article ‘Deconstructing Morphology’

Scholtz G. in press. A plea for ‘genealogical thinking’ in comparative biology – a rebuttal to the reply of Szucsich, Wirkner, and Pass to my article ‘Deconstructing Morphology’. —Acta Zoologica (Stockholm) 00 : 1–4. Szucsich et al. (in press) claim that – in contrast to my statement – morphological thinking has to be ‘cladistic.’ Based on this premise, they stress the difference between the relationships among states of characters versus those among structures assigned to the same character state as implemented in numerical cladistic reasoning. SEA claim that my approach to the homology concept only deals with the problem of the integration of various character states into the same character, whereas the necessary relationships among structures assigned to the same state are not covered. Based on this distinction, SEA also criticise the application of similarity in my definition of homology. Furthermore, they address the issue of evolutionarily independent units.     

On some aspects of parallel evolution in Chelicerata

A study is made of some aspects of parallel evolution in Chelicerata. Definitions are given of parallel evolution, convergence, homology and analogy. It is pointed out that the concept of parallel evolution (parallelism) is initially formed in an empirical way, and that a judgment must be based on formal criteria. Particular attention is paid to the rôle of gene regulation in parallel evolution, to the special case of convergence as a result of heterologous regulatory mechanisms, to parallel evolution in homonomous structures (and the superposition of parallelisms and divergences), and to parallelism in the evolution of characters used in higher classification.     

On the necessity of an archetypal concept in morphology: With special reference to the concepts of “structure” and “homology”

Morphological elements, or structures, are sorted into four categories depending on their level of anatomical isolation and the presence or absence of intrinsically identifying characteristics. These four categories are used to highlight the difficulties with the concept of structure and our ability to identify or define structures. The analysis is extended to the concept of homology through a discussion of the methodological and philosophical problems of the current concept of homology. It is argued that homology is fundamentally a similarity based concept rather than a phylogenetic concept, and a proposal is put forth to return to a comparative context for homology. It is shown that for both the concepts of structure and homology ana priori assumption of stable underlying patterns (i.e. archetypes) is essential.