The notion of homology in current comparative biology

Current notions on homology, and its recognition, causation, and explanation are reviewed in this report. The focus is primarily on concepts because the formulation of precise definitions of homology has contributed little to our understanding of the issue. Different aspects or concepts of homology have been contrasted, currently the most important ones being the distinction between systematic and biological concepts. The systematic concept of homology focuses on common ancestry and on taxa; the biological concept tries to explain patterns of conservatism in evolution by shared developmental constraints. Similarity or correspondence is generally accepted as a primary criterion in the delimitation of homologues, albeit that this criterion is not without practical and theoretical problems. Apart from similarity, the biological concept of homology also stresses developmental individuality of putative homologous structures. Structural and positional aspects of homology can be separated, with positional homology acquiring an independent status. Similarity, topographic relationships, and ontogenetic development cannot be tests of homology. Within the cladistic paradigm, the most decisive test of homology is that of congruence; proponents of the biological-homology concept have been less concerned with test implications. Adopting a hierarchical view of nature suggests that characters have to be homologized at their appropriate level of organization. A taxic or systematic approach to homology has precedence over a transformational or biological approach. Nevertheless, pattern analysis and process explanations are not independent of each other.     

Historical Patterns of Developmental Integration in Piranhas

TO test the hypothesis that developmental integration coordinatesevolutionary change through history, we dissect the spatialand temporal integration of ontogenetic allometries of piranhabody form and examine the evolutionary coordination among ontogeneticfeatures by a phylogenetic analysis. Few of our characters provideevidence in support of the hypothesis. In general, we find thatdevelopmental integration is historically labile, being modifiedat virtually every speciation event. Most of the ontogeneticfeatures are dissociated in their phylogenetic changes and evolvein a mosaic fashion. Indeed, developmental integration is solabile that primitively integrated features of ontogeny usuallyevolve subsequently as independent characters. Evolutionarychanges in developmental integration can result in increasedor decreased integration on the ontogenetic time scale. Whenlocalized features are deleted from ontogeny, or when spatiallyintegrated features are gained, the derived ontogenies may bemore integrated in a spatial sense. The end result of phylogeneticdissociations may be a more highly developmentally integratedontogeny. Thus, in the piranhas we studied, we find a historicallycoupled increase in developmental integration caudally and adecrease indevelopmental integration cranially.     

Phylogenetic interpretation of ontogenetic change: sorting out the actual and artefactual in an empirical case study of centrarchid fishes

Hypothesized relationships between ontogenetic and phylogenetic change in morphological characters were empirically tested in centrarchid fishes by comparing observed patterns of character development with patterns of character evolution as inferred from a representative phylogenetic hypothesis. This phylogeny was based on 56–61 morphological characters that were polarized by outgroup comparison. Through these comparisons, evolutionary changes in character ontogeny were categorized in one of eight classes (terminal addition, terminal deletion, terminal substitution, non-terminal addition, non-terminal deletion, non-terminal substitution, ontogenetic reversal and substitution). The relative frequencies of each of these classes provided an empirical basis from which assumptions underlying hypothesized relationships between ontogeny and phylogeny were tested. In order to test hypothesized relationships between ontogeny and phylogeny that involve assumptions about the relative frequencies of terminal change (e.g. the use of ontogeny as a homology criterion), two additional phylogenies were generated in which terminal addition and terminal deletion were maximized and minimized for all characters. Character state change interpreted from these phylogenies thus represents the maxima and minima of the frequency range of terminal addition and terminal deletion for the 8.7 × 10³⁶ trees possible for centrarchids. It was found for these data that terminal change accounts for c. 75% of the character state change. This suggests either that early ontogeny is conserved in evolution or that interpretation and classification of evolutionary changes in ontogeny is biased in part by the way that characters are recognized, delimited and coded. It was found that ontogenetic interpretation is influenced by two levels of homology decision: an initial decision involving delimitation of the character (the ontogenetic sequence), and the subsequent recognition of homologous components of developmental sequences. Recognition of phylogenetic homology among individual components of developmental sequences is necessary for interpretation of evolutionary changes in ontogeny as either terminal or non-terminal. If development is the primary criterion applied in recognizing individual homologies among parts of ontogenetic sequences, the only possible interpretation of phylogenetic differences is that of terminal change. If homologies of the components cannot be ascertained, recognition of the homology of the developmental sequence as a whole will result in the interpretation of evolutionary differences as substitutions. Particularly when the objective of a study is to discover how ontogeny has evolved, criteria in addition to ontogeny must be used to recognize homology. Interpretation is also dependent upon delimitation within an ontogenetic sequence. This is in part a function of the way that an investigator ‘sees’ and codes characters. Binary and multistate characters influence interpretation differently and predictably. The use of ontogeny for determining phylogenetic polarity as previously proposed rests on the assumptions that ancestral ontogenies are conserved and that character evolution occurs predominantly through terminal addition. It was found for these data that terminal addition may comprise a maximum of 51.9% of the total character state change. It is concluded that the ontogenetic criterion is not a reliable indicator of phylogenetic polarity. Process and pattern data are collected simultaneously by those engaged in comparative morphological studies of development. The set of alternative explanatory processes is limited in the process of observing development. These form necessary starting points for the research of developmental biologists. Separating ‘empirical’ results from interpretational influences requires awareness of potential biases in the course of character selection, coding and interpretation. Consideration of the interpretational problems involved in identifying and classifying phylogenetic changes in ontogeny leads to a re-evaluation of the purpose, usefulness and information conveyed by the current classification system. It is recommended that alternative classification schemes be pursued.     

Homology of Hox Genes and the Zootype Concept in Early Metazoan Evolution

The correct identification of homologous Hox genes within and between diplo- and triploblastic animals is of crucial importance for recent hypotheses on the anagenetic evolution of animal bauplans. While the homology discussion in general has reached new heights, we apply traditional homology criteria to assign homology to Hox genes from diploblastic animals. Comparison of theTrox-2gene from the presumably most basal metazoan animal, the placozoanTrichoplax adhaerens,to other Hox genes suggests the presence of unambiguous homologs in Hydrozoa and Scyphozoa and the absence of any specific homolog in triploblasts. Furthermore, the comparisons provide support for the idea that Hox genes—at least in diploblastic animals—are composed of functional subunits (modules), which to some degree have undergone independent evolution. The findings are not readily compatible with the existence of the “zootype” in diploblastic animals.     

ONTOGENETIC VARIATION IN PATTERNS OF DEVELOPMENTAL AND FUNCTIONAL INTEGRATION IN SKULLS OF SIGMODON FULVIVENTER

Patterns of variation and covariation within populations can influence how characters respond to natural selection and random genetic drift and so constrain the ability of natural selection to modify the phenotype. We examined several potential developmental and functional explanations of character covariation throughout ontogeny using known-age samples of the cotton rat (Sigmodon fulviventer) to identify the causes of covariation and to assess the variability of patterns of covariation throughout postnatal growth. Competing developmental and functional models were fit to samples of orofacial and neurocranial measures by confirmatory factor analysis and evaluated for their ability to reconstruct observed variance-covariance matrices. Samples of successive ages were simultaneously fit to a common model to test the hypothesis that the patterns of developmental and functional integration were invariant between ages. Orofacial characters derived from the same branchial-arch primordium covary early in ontogeny. Subsequently, there is a repatterning of integration that may reflect a transition from developmental to functional sources of integration. Neurocranial characters exhibit even more variation in patterns of covariation: initially, characters appear to comprise a single integrated unit; before puberty, they appear to respond to localized bone growth; after puberty, they form separate calvarial and basicranial components. This ontogenetic variation in patterns of covariation suggests that developmental constraints are transient and flexible and that the consequences of selection may depend upon the age at which it acts.     

DISSECTION OF EVOLUTIONARY NETWORKS TO ASSESS THEIR ROLE IN THE EVOLUTION OF ROBUSTNESS,FUNCTION, AND DIVERSIFICATION

Biological systems are remarkably robust in the face of environmental, mutational, and developmental perturbations. Analyses of molecular networks reveal recurrent features, such as modularity, that have been implicated in robustness and evolvability. Multiple theoretical models account for these features, yet few empirical tests of these models exist. Here I develop a set of broadly applicable methodologies to enable expanded empirical evaluation of model predictions. The methodologies focus on the inference and analysis of networks that depict evolutionary correlations among characters. I apply these methodologies to analyze an evolutionary network at a larger scale of organization among 42 stem anatomical and morphological characters of 52 species in the genus Adenia (Passifloraceae). I evaluate a model predicting that modular evolutionary networks will evolve in response to environmental change. The evolutionary network of Adenia is modular and “small‐world,” and the three diagnosed modules correspond roughly to functions of transport, storage, and mechanical support. The phylogenetically informed analyses suggest that the storage module is more impacted by environmental change than expected by chance. These results corroborate the hypothesis that modularity reduces the impact of environmental change, but this result requires further empirical evaluation that can be aided by the proposed methods in additional study systems.     

Walter Garstang: a retrospective

Although, Walter Garstang died over 60 years ago, his work is still cited—sometimes praised, but sometimes belittled. On the negative side, he often appropriated ideas of others without attribution, ignored earlier studies conflicting with his theories, and clung to notions like inheritance of acquired characters, progressive evolution, and saltation after many of his contemporaries were advancing toward the modern synthesis. Moreover, his evolutionary scenarios—especially his derivation of vertebrates from a sessile ascidian—have not been well supported by recent work in developmental genetics and molecular phylogenetics. On the positive side, Garstang firmly established several points of view that remain useful in the age of evolutionary development (evo-devo). He popularized the valid idea that adaptive changes in larvae combined with shifts in developmental timing (heterochrony) could radically change adult morphology and provide an escape from overspecialization. Moreover, his re-statement of the biogenetic law is now widely accepted: namely, that recapitulation results when characters at one stage of development are required for the correct formation of other characters at subsequent stages (his stepping stone model). In other words, ontogeny creates phylogeny because some developmental features are constraints, favoring particular evolutionary outcomes while excluding others. This viewpoint is a useful basis for advancing concepts of homology and for comparing the phylogeny of ontogenies across a series of animals to ascertain the timing and the nature of the underlying ontogenetic changes.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

The ontogenetic complexity of developmental constraints

Developmental constraint is a theoretically important construct bridging ontogenetic and evolutionary studies. We propose a new operationalization of this notion that exploits the unusually rich measurement structure of landmark data. We represent landmark configurations by their partial warps, a basis for morphospace that represents a set of localized features of form. A finding of developmental constraint arises from the interplay between age-varying means and age-specific variances in these subspaces of morphospace. Examination of variances and means in 16 ventral skull landmarks in the cotton rat S. fulviventer at ages 1, 10, 20, and 30 days yielded three types of developmental constraint: canalization (constraint to relatively constant form age by age); chreods (reduction of variance orthogonal to the mean trajectory over ages); and opposition (reduction of age-specific variance along the mean trajectory over ages). While canalization and chreodic constraints have been noted previously, the oppositional type of constraint appears novel. Only one of our characters, relative length and orientation of the incisive foramen, appears to be canalized. Although skull growth becomes increasingly integrated through ontogeny, our characters display a remarkable spatiotemporal complexity in patterns of variance reduction. The specific assortment of constraints observed may be related to the precociality of Sigmodon. We suggest that Waddington's diagrammatic presentation of the “epigenetic landscape” may be misleading in quantitative studies of developmental regulation.     

Quantitative genetics of butterfly wing color patterns

Developmental processes exert their influence on the evolution of complex morphologies through the genetic correlations they engender between traits. Butterfly wing color patterns provide a model system to examine this connection between development and evolution. In butterflies, the nymphalid groundplan is a framework used to decompose complex wing patterns into their component pattern elements. The first goal of this work has been to determine whether the components of the nymphalid groundplan are the products of independent developmental processes. To test this hypothesis, the genetic correlation matrices for two species of butterflies, Precis coenia and Precis evarete, were estimated for 27 wing pattern characters. The second purpose was to test the hypothesis that the differentiation of serial homologs lowers their genetic correlations. The “eyespots” found serially repeated across the fore- and hindwing and on the dorsal and ventral wing surfaces provided an opportunity to test this hypothesis. The genetic correlation matrices of both species were very similar. The pattern of genetic correlation measured between the different types of pattern elements and between the homologous repeats of a pattern element supported the first hypothesis of developmental independence among the elements of the groundplan. The correlation pattern among the differentiated serial homologs was similarly found to support the second hypothesis: pairs of eyespots that had differentiated had lower genetic correlations than pairs that were similar in morphology. The implications of this study are twofold: First, the apparent developmental independence among the distinct elements of wing pattern has facilitated the vast diversification in morphology found in butterflies. Second, the lower genetic correlations betweendifferentiated homologs demonstrates that developmental constraints can in fact be broken. The extent to which genetic correlations readily change, however, remains unknown. © 1994 Wiley-Liss, Inc.     

Opercular development and ontogenetic re-organization in a direct-developing frog

The direct-developing frog, Eleutherodactylus coqui, has eliminated the tadpole stage from its ontogeny, and lacks many larval characters. We demonstrate that the dermal folds of E. coqui are homologous with the opercular folds of metamorphosing frogs. In both E. coqui and its metamorphic counterparts the opercular folds grow over the developing forelimb before perforating to free the entrapped limb. Opercular perforation in E. coqui occurs even in the absence of the forelimb but shows no signs of thyroid hormone dependence. The condensation of E. coqui development appears due to the excision of the extended larval period of developmental stasis. Analysis of opercular development, when viewed in conjunction with other developmental characters, suggests the ontogenetic period in the ancestral Eleutherodactylus life-history from which the tadpole was likely eliminated. Received: 7 October 1999 / Accepted: 17 January 2000     

DEVELOPMENT,FUNCTION, AND THE QUANTITATIVE GENETICS OF WING MELANIN PATTERN IN PIERIS BUTTERFLIES

Do genetic correlations among phenotypic characters reflect developmental organization or functional coadaptation of the characters? We test these hypotheses for the wing melanin pattern of Pieris occidentalis butterflies, by comparing estimated genetic correlations among wing melanin characters with a priori predictions of the developmental organization and the functional (thermoregulatory) organization of melanin pattern. There were significant broad-sense heritabilities and significant genetic correlations for most melanin characters. Matrix correlation tests revealed significant agreement between the observed genetic correlations and both developmental and functional predictions in most cases; this occurred even when the overlap between developmental and functional predictions was eliminated. These results suggest that both developmental organization and functional coadaptation among melanin characters influence the genetic correlation structure of melanin pattern in this species. These results have two important implications for the evolution of melanin pattern in P. occidentalis and other butterflies: 1) most phenotypic variation in pattern may reflect variation among, rather than within, sets of developmentally homologous wing melanin characters; and 2) in a changing selective environment, genetic correlations may retard the disruption of functionally coupled melanin characters, thus affecting the evolutionary response to selection.     

ONTOGENY OF THE PALEOZOIC OVULE,CALLOSPERMARION PUSILLUM

The ontogeny of the upper Pennsylvanian age gymnospermous ovule, Callospermarion pusillum, is described from petrifaction specimens collected at the Berryville locality in Illinois. Ovules exhibit a wide range of dimensional and structural features that indicate an extensive developmental sequence. Specimens range from ovules with indistinct zonation of the thin-walled integument to those with thick-walled cells of the sclerotesta. The apex of the fleshy nucellus in some specimens is preserved as a cellular mound, while in others a well-formed cellular pollen chamber is present; still other ovules are characterized by a papery-thin nucellus and pollen chamber wall. The megagametophyte of most specimens is represented by a hollow megaspore membrane that may be restricted to the base of the nucellus, or occupy the entire seed cavity. In a few specimens cellular gametophytes are preserved, and in one ovule archegonia with supposed eggs are also present. Variability in each of the features is compared with ontogenetic changes in comparable structures of living gymnospermous ovules and is correlated with ovule size. A developmental sequence for the fossil ovules is proposed.     

Embryonic expression of the single Tribolium engrailed homolog

We have cloned and sequenced the single Tribolium homolog of the Drosophila engrailed gene. The predicted protein contains a homeobox and several domains conserved among all engrailed genes identified to date. In addition it contains several features specific to the invected homologs of Bombyx and Drosophila, indicating that these features most likely were present in the ancestral gene in the common ancestor of holometabolous insects. We used the cross-reacting monoclonal antibody, 4D9, to follow the expression of the Engrailed protein during segmentation in Tribolium embryos. As in other insects, Engrailed accumulates in the nuclei of cells along the posterior margin of each segment. The first Engrailed stripe appears as the embryonic rudiment condenses. Then as the rudiment elongates into a germ band, Engrailed stripes appear in an anterior to posterior progression, just prior to morphological evidence of the formation of each segment. As in Drosophila (a long germ insect), expression of engrailed in Tribolium (classified as a short germ insect) is preceeded by the expression of several homologous segmentation genes, suggesting that similar genetic regulatory mechanisms are shared by diverse developmental types. © 1994 Wiley-Liss, Inc.     

Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles

Snakes possess a derived anatomy, characterized by limb reduction and reorganization of the skull and internal organs. To understand the origin of snakes from an ontogenetic point of view, we conducted comprehensive investigations on the timing of skeletal elements, based on published and new data, and reconstructed the evolution of the ossification sequence among squamates. We included for the first time Varanus, a critical taxon in phylogenetic context. There is comprehensive delay in the onset of ossification of most skeletal elements in snakes when compared to reference developmental events through evolution. We hypothesize that progressing deceleration accompanied limb reduction and reorganization of the snake skull. Molecular and morphological studies have suggested close relationship of snakes to either amphisbaenians, scincids, geckos, iguanids, or varanids. Likewise, alternative hypotheses on habitat for stem snakes have been postulated. Our comprehensive heterochrony analyses detected developmental shifts in ossification for each hypothesis of snake origin. Moreover, we show that reconstruction of ancestral developmental sequences is a valuable tool to understand ontogenetic mechanisms associated with major evolutionary changes and test homology hypotheses. The “supratemporal” of snakes could be homolog to squamosal of other squamates, which starts ossification early to become relatively large in snakes.     

THE EVOLUTION OF ELONGATE SHAPE IN DIATOMS1

Diatoms have been classified historically as either centric or pennate based on a number of features, cell outline foremost among them. The consensus among nearly every estimate of the diatom phylogeny is that the traditional pennate diatoms (Pennales) constitute a well‐supported clade, whereas centric diatoms do not. The problem with the centric–pennate classification was highlighted by some recent analyses concerning the phylogenetic position of Toxarium, whereby it was concluded that this “centric” diatom independently evolved several pennate‐like characters including an elongate, pennate‐like cell outline. We performed several phylogenetic analyses to test the hypothesis that Toxarium evolved its elongate shape independently from Pennales. First, we reanalyzed the original data set used to infer the phylogenetic position of Toxarium and found that a more thorough heuristic search was necessary to find the optimal tree. Second, we aligned 181 diatom and eight outgroup SSU rDNA sequences to maximize the juxtapositioning of similar primary and secondary structure of the 18S rRNA molecule over a much broader sampling of diatoms. We then performed a number of phylogenetic analyses purposely based on disparate sets of assumptions and found that none of these analyses supported the conclusion that Toxarium acquired its pennate‐like outline independently from Pennales. Our results suggest that elongate outline is congruent with SSU rDNA data and may be synapomorphic for a larger, more inclusive clade than the traditional Pennales.     

How can a character be developmentally constrained despite variation in developmental pathways?

A fundamental riddle of evolutionary developmental biology is the conservation of adult morphological patterns (Hall, 1992). Conservative patterns are either called body plans if they concern overall body design, or homologues if they concern parts of the body (Riedl, 1978; Roth, 1982; Sattler, 1984; Van Valen, 1982; Wagner, 1989a, 1989b). An adult pattern is considered conservative if it remains unchanged in spite of changes in function, as indicated by the original definition of homology by Owen, as a similarity of organs regardless of form and function (Owen, 1848). Conservation of anatomical features despite different adaptive pressures is naturally explained by developmental constraints (Wagner, 1986). However, this approach to explain the biological basis of homology is plagued by the fact that developmental pathways are often more variable than the characters that they produce (see Tab. 1) (Hall, 1992; Roth, 1988, 1991; Spemann, 1915; Wagner, 1989b). This is also true for any other application of the concept of developmental constraints. The widely held opinion that early stages of development are conservative because any early perturbation is likely to interfere with later development, is far from absolute, since a vast amount of data in comparative developmental biology speaks to developmental variation (see e.g. the examples in Tab. 1). The question then is, how can developmental constraints on adult variation be reconciled with the fact of developmental variation?     

CENTRORADIALIS/TERMINAL FLOWER 1 gene homolog is conserved inN. tabacum, a determinate inflorescence plant

A mutation in theCENTRORADIALIS (CEN) gene ofAntirrhinum and in theTERMINAL FLOWER 1 (TFL1) gene ofArabidopsis causes their indeterminate inflorescence to determinate. We clonedCEN/TFL1 homologs fromNicotiana tabacum, the wild-type of which has a determinate inflorescence. TheCEN gene was expressed in the inflorescnece meristem and kept its inflorescence meristem identity, whereas the tobacco homolog (NCH) was expressed at a low level throughout the plant’s development. AlthoughCEN andNCH are highly homologous genes, they may have been recruited to different developmental functions during their evolution. TwoNCH genes are derived from amphidiploidN. tabacum, but both of them hybridized with its diploid parents,N. sylvestris andN. tomentosiformis. Southern blotting, and the genomic organization ofTFL1 inArabidopsis revealed that anotherCEN homolog exists in the genome ofArabidopsis. These results suggest that there are two copies of theCEN homolog per diploid plant. The extended abstract of a paper presented at the 13th International Symposium in Conjugation with Award of the International Prize for Biology “Frontier of Plant Biology” These two authors contributed to this work equally.     

Chromosome territory arrangement and homologous pairing in nuclei of <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> are predominantly random except for NOR-bearing chromosomes

Differential painting of all five chromosome pairs of Arabidopsis thaliana revealed for the first time the interphase chromosome arrangement in a euploid plant. Side-by-side arrangement of heterologous chromosome territories and homologous association of chromosomes 1, 3 and 5 (on average in 35–50% of nuclei) are in accordance with the random frequency predicted by computer simulations. Only the nucleolus organizing region (NOR)-bearing chromosome 2 and 4 homologs associate more often than randomly, since NORs mostly attach to a single nucleolus. Somatic pairing of homologous 100 kb segments occurs less frequently than homolog association, not significantly more often than expected at random and not simultaneously along the homologs. Thus, chromosome arrangement in Arabidopsis differs from that in Drosophila (characterized by somatic pairing of homologs), in spite of similar genome size, sequence organization and chromosome number. Nevertheless, in up to 31.5% of investigated Arabidopsis nuclei allelic sequences may share positions close enough for homologous recombination.Electronic Supplementary Material Supplementary material is available for this article at .