Rejecting "the given" in systematics

How morphology and systematics come together through morphological analysis, homology hypotheses and phylogenetic analysis is a topic of continuing debate. Some contemporary approaches reject biological evaluation of morphological characters and fall back on an atheoretical and putatively objective (but, in fact, phenetic) approach that defers to the test of congruence for homology assessment. We note persistent trends toward an uncritical empiricism (where evidence is believed to be immediately “given” in putatively theory‐free observation) and instrumentalism (where hypotheses of primary homology become mere instruments with little or no empirical foundation for choosing among competing phylogenetic hypotheses). We suggest that this situation is partly a consequence of the fact that the test of congruence and the related concept of total evidence have been inappropriately tied to a Popperian philosophy in modern systematics. Total evidence is a classical principle of inductive inference and does not imply a deductive test of homology. The test of congruence by itself is based philosophically on a coherence theory of truth (coherentism in epistemology), which is unconcerned with empirical foundation. We therefore argue that coherence of character statements (congruence of characters) is a necessary, but not a sufficient, condition to support or refute hypotheses of homology or phylogenetic relationship. There should be at least some causal grounding for homology hypotheses beyond mere congruence. Such causal grounding may be achieved, for example, through empirical investigations of comparative anatomy, developmental biology, functional morphology and secondary structure. © The Willi Hennig Society 2006.     

Quantitative tests of primary homology

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

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.     

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.     

Homology and ontogeny: pattern and process in comparative developmental biology

In this article the interface between development and homology is discussed. Development is here interpreted as a sequence of evolutionarily independent stages. Any approach stressing the importance of specific developmental stages is rejected. A homology definition is favoured which includes similarity, and complexity serves as a test for homology. Complexity is seen as the possibility of subdividing a character into evolutionarily independent corresponding substructures. Topology as a test for homology is critically discussed because corresponding positions are not necessarily indicative of homology. Complexity can be used twofold for homology assessments of development: either stages or processes of development are homologised. These two approaches must not be conflated. This distinction leads to the conclusion that there is no ontogenetic homology “criterion”.     

Transformation Series as an Ideographic Character Concept

An ideographic concept of character is indispensable to phylogenetic inference. Hennig proposed that characters be conceptualized as “transformation series”, a proposal that is firmly grounded in evolutionary theory and consistent with the method of inferring transformation events as evidence of phylogenetic propinquity. Nevertheless, that concept is usually overlooked or rejected in favor of others based on similarity. Here we explicate Hennig's definition of character as an ideographic concept in the science of phylogenetic systematics. As transformation series, characters are historical individuals akin to species and clades. As such, the related concept of homology refers to a historical identity relation and is not equivalent to or synonymous with synapomorphy. The distinction between primary and secondary homology is dismissed on the grounds that it conflates the concept of homology with the discovery operations used to detect instances of that concept. Although concern for character dependence is generally valid, it is often misplaced, focusing on functional or developmental correlation (both of which are irrelevant in phylogenetic systematics but may be valid in other fields) instead of the historical/transformational independence relevant to phylogenetic inference. As an ideographic science concerned with concrete objects and events (i.e. individuals), intensionally and extensionally defined properties are inconsistent with the individuation of characters for phylogenetic analysis, the utility of properties being limited to communicating results and facilitating future rounds of testing.     

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.     

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.     

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.     

DEVELOPMENTAL CORRELATES OF GENOME SIZE IN PLETHODONTID SALAMANDERS AND THEIR IMPLICATIONS FOR GENOME EVOLUTION

We present an analysis of the evolutionary relationship between genome size (C-value, mass of DNA per haploid nucleus) and developmental rate using observations of limb regeneration in salamanders of the family Plethodontidae. Rates of growth and differentiation of regenerating limbs are reported for 27 plethodontid species whose C-values range from 14 to 76 picograms. A phylogenetic analysis employing Felsenstein's method of independent contrasts indicates that rate of differentiation is inversely proportional to genome size, although we have not identified any statistically significant association between genome size and the growth rate of regenerating tissue. Our results are consistent with an interpretation that genome size may place a limit on the maximum rate of regeneration attainable in plethodontid salamanders. The implications of our findings for the “junk DNA,” “nucleotypic DNA,” “selfish DNA,” and “skeletal DNA” hypotheses of genome evolution are discussed.     

Good characters and homology

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

Modules, kinds, and homology

Developmental modules are best conceptualized as homeostatic property cluster natural kinds. As is true in other fields of biology, an individual may instantiate properties of various natural kinds. Through their dissociability, developmental modules can be recruited to function as evolutionary modules. The proper analogy to developmental modules, atoms, or biological species depends on the scope over which specific developmental modules allow generalizations. The nature of the relationship between developmental modules, evolutionary modules, and taxic (phylogenetic) homology are explored. Similarity of gene expression patterns and developmental pathways as captured by biological homology may support hypotheses of taxic homology, but not the other way around.     

The phylogenetic relevance of thoracic musculature: a case study including a description of the thorax anatomy of Zygoptera (Insecta: Odonata) larvae

New morphological techniques allow for the evaluation of novel character systems that are potentially important for phylogenetic analysis. Only a few studies so far have used character systems from the insect thorax for phylogenetics; the reasons for this might include a lack of common terminology or established homology for pterygote insect thorax musculature. Still, recent studies have proposed common terminology and hypotheses of homology, now allowing for an evaluation of thoracic morphological character systems among the groups of winged insects. Using X ‐ray microtomography (μCT) we present a detailed study of the thorax musculature of O donata as an important phylogenetic character system, with a matrix of 298 characters with 697 character states, including novel data from the thoracic anatomy of eight damselfly larvae. We also included additional O donata, E phemeroptera and N eoptera taxa from the literature and demonstrate the phylogenetic relevance of this character system by reproducing phylogenetic topologies of established relationships. We also compared high‐resolution data from O donata larvae from our study and from recent literature with data from older literature in the adult O donata. All major clades were successfully recovered, (e.g. O donata, E piprocta, A nisoptera and Z ygoptera) with high node support, but obtained higher phylogenetic resolution with the larval data. The best phylogenetic resolution was achieved by combining the adult and larval characters. The taxon sampling and character matrix is the largest to date and underlines the potential relevance of the thorax musculature as an important phylogenetic character system.     

Revisiting the Darwinian shortfall in biodiversity conservation

Among the seven shortfalls of biodiversity knowledge, the one that makes direct reference to phylogenetic information is the Darwinian shortfall, which embraces three components: “(1) the lack of fully resolved phylogenies for most groups of organisms; (2) the limited knowledge of branch lengths and difficulties in absolute time calibrations; and (3) unknown evolutionary models linking those phylogenies to ecological traits and the life-history variation” (Diniz-Filho et al. in Trends Ecol Evol 28:689–694, 2013). In order to overcome them, Diniz-Filho et al. (Trends Ecol Evol 28:689–694, 2013) emphasized the need to know the problems relative to phylogeny reconstruction, but they did not provide a clear comprehension of these problems. In the present article, I aim to comment on these problems in the context of the five epistemic stages of phylogenetic analysis. These are: (1) taxon sampling; (2) evidence; (3) homology assessment; (4) optimization methods; and (5) hypotheses formulation. A brief review of these stages is necessary to comprehend how complex is the use of phylogenetic hypotheses in ecology and conservation. I also provide additional and balanced solutions in an attempt to overcome the evolutionary shortfall.     

Evolution of the claustrum in Cnidaria: comparative anatomy reveals that it is exclusive to some species of Staurozoa and absent in Cubozoa

The claustrum in Cnidaria is a tissue in the gastrovascular cavity delimited by a central layer of mesoglea surrounded by gastrodermis (i.e., gastrodermis-mesoglea-gastrodermis), without communication with epidermis. By dividing the gastrovascular cavity, the four claustra provide an additional level of complexity. The presence of claustra in Cubozoa and Staurozoa has been used as evidence supporting a close relationship between these two cnidarian classes. However, the detailed anatomy of the claustrum has never been comparatively analyzed, rendering the evolution of this character among Cnidaria and its homology in Staurozoa and Cubozoa uncertain. This study provides a comparative investigation of the internal anatomy of the claustrum in Staurozoa and Cubozoa, addressing its evolutionary history based on recent phylogenetic hypotheses for Cnidaria. We conclude that the claustrum is a character exclusive to some species of Staurozoa, with a homoplastic evolution in the class, and that the structure called the “claustrum” in Cubozoa corresponds to the valve of gastric ostium, a structure at the base of the manubrium, which is also present in Staurozoa with and without claustrum. Thus, the claustrum cannot be a synapomorphy of a hypothetical clade uniting Staurozoa and Cubozoa, nor can its hypothetical presence in enigmatic fossils be used to support cubozoan affinities.     

Not deconstructing serial homology,but instead,the a priori assumption that it generally involves ancestral anatomical similarity: An answer to Kuznetsov's paper

I am very thankful to Kuznetsov for his comments on our recent paper about serial structures published in this journal. I hope this is just the beginning of a much wider, and holistic, discussion on the evolution of serial homologous structures, and of so-called “serial structures” in general, whether they are truly serial homologs or the secondary result of homoplasy. Strangely, Kuznetsov seems to have missed the main point of our paper, what is particularly puzzling as this point is clearly made in the very title of our paper. For instance, he states that “Siomava et al. claim that the serial homologues are false because they are ancestrally anisomeric (dissimilar)' and that” Siomava et al., (Siomava et al., Journal of Morphology, 2020, 281, 1110–1132) expected that if serial homology was true, then the serial homologs would be identical at the start and then only diverge. “ However, our paper clearly did not state this. Instead, we stated that (a) serial homology is a real phenomenon, and (b) ancestral dissimilarity is actually likely the norm, and not the exception, within serial homology. In particular, our paper showed that, as clearly stated in its title and abstract, within the evolution of serial homologues these structures “many times display trends toward less similarity while in many others display trends toward more similarity, that is, one cannot say that there is a clear, overall trend to anisomerism.” Serial homology is therefore a genuine and much widespread phenomenon within the evolution of life in this planet. It is clearly one of the most important issues—and paradoxically one of the less understood, precisely because of the a priori acceptance of long-standing assumptions that have never been empirically tested, some of them repeated in Kuznetsov's paper—within macroevolution and comparative anatomy.     

Hennig's semaphoront concept and the use of ontogenetic stages in phylogenetic reconstruction

A new practice in systematics, “semaphoront” coding, treats developmental stages as terminals, and it derives from Hennig's concept of the same name. Semaphoront coding has been implemented recently by Lamsdell and Selden (BMC Evol. Biol., 2013, 13:98) and Wolfe and Hegna (Cladistics, 2014, 30:366) in an effort to understand the relationships of fossil taxa of unknown developmental stage. We submit that this approach is antithetical to cladistic practice and constitutes a gross misunderstanding of Hennig's original idea. Here we review the concept of the semaphoront and clarify the role of the semaphoront in phylogenetic systematics. We contend that treating ontogenetic stages as terminals both violates tenets of phylogenetic systematics and oversimplifies the complexity of developmental processes. We advocate Hennig's alternative of including data from as many semaphoronts as possible, but implemented using the superior total evidence framework. Finally, we contend that the application of semaphoront coding to any palaeontological question requires invoking multiple, unjustified assumptions, and ultimately will not yield a possible phylogenetic solution. A total evidence approach can grapple with the placement of fossil developmental stages, if only imperfectly.