The role of parsimony,outgroup analysis,and theory of evolution in phylogenetic systematics

It is argued that both the principle of parsimony and the theory of evolution, especially that of natural selection, are essential analytical tools in phylogenetic systematics, whereas the widely used outgroup analysis is completely useless and may even be misleading. In any systematic analysis, two types of patterns of characters and character states must be discriminated which are referred to as completely and incompletely resolved. In the former, all known species are presented in which the characters and their states studied occur, whereas in the latter this is not the case. Dependent on its structure, a pattern of characters and their states may be explained by either a unique or by various conflicting, equally most parsimonious hypotheses of relationships. The so-called permutation method is introduced which facilitates finding the conflicting, equally most parsimonious hypotheses of relationships. The utility of the principle of parsimony is limited by the uncertainty as to whether its application in systematics must refer to the minimum number of steps needed to explain a pattern of characterts and their states most parsimoniously or to the minimum number of evolutionary events assumed to have caused these steps. Although these numbers may differ, the former is usually preferred for simplicity. The types of outgroup analysis are shown to exist which are termed parsimony analysis based on test samples and cladistic type of outgroup analysis. Essentially, the former is used for analysing incompletely resolved patterns of characters and their states, the latter for analysing completely resolved ones. Both types are shown to be completely useless for rejecting even one of various conflicting, equally most parsimonious hypotheses of relationships. According to contemporary knowledge, this task can be accomplished only by employing the theory of evolution (including the theory of natural selection). But even then, many phylogenetic-systematic problems will remain unsolved. In such cases, arbitrary algorithms like those offered by phenetics can at best offer pseudosolutions to open problems. Despite its limitations, phylogenetic systematics is superior to any kind of aphylogenetic systematics (transformed cladistics included) in approaching a (not: the) “general reference system” of organisms.     

Grundsätze der phylogenetischen Systematik (Eine praxisorientierte Übersicht)

The essential elements of phylogenetic systematics in the sense of Hennig are emphasized: The search for synapomorphies based on a special method of comparative morphology, and the aim of an exclusive use of synapomorphies for kinship proof and the basis of systematics. Special aspects of comparative morphology are: “Directed comparisons” steady reciprocal reflection between comparative morphological result and the system methodical efforts for the realization of distinctive details, comprehensive documentation and functional interpretation. This is equally true for recent and fossil forms. Most suitable for the method (in the sense defined above) are groups with numerous differentiated morphological characters, which can also be preserved in the fossil state. The less this is the case the less is the chance for achieving necessary numbers of well proven synapomorphies. Even so, it is not permitted—for those who want to perform phylogenetic systematics in the sense of Hennig—to use convergences, parallelisms or symplesiomorphies in the sense of “synapomorphies” as phylogenetic arguments for kinship relations. Numerous examples and diagrams demonstrate the methodological proceeding, and differences towards other methods of phylogenetical reconstruction and interpretation. Special attention is paid to direct and indirect conclusions drawn from fossils: Time of origin of characters, stem groups and *groups; predictions concerning the appearance (set of characters) of fossils and simultaneous existence of “neighbour groups” (sister groups, and more distantly related taxa).     

Variable and Invariable DNA Repeat Characters Revealed by Taxonprint Approach Are Useful for Molecular Systematics

A specially optimized restriction analysis of highly repetitive DNA elements, called DNA taxonprint, was applied for phylogenetic study of primates and lizards. It was shown that electrophoretic bands of DNA repeats revealed by the taxonprint technique have valuable properties for molecular systematics. Approximately half of taxonprint bands (TB) are invariable and do not disappear from the genomes during evolution or change spontaneously. Presumably these invariable bands are restriction fragments of dispersed DNA repeats. Another group represents variable taxonprint bands that differ even between closely related species. These variable bands are probably represented by tandem DNA repeats and could be used as species-specific markers. It was shown that taxonprint bands are independent characters since the appearance of a new taxonprint band does not change the previous band pattern. Phylogenetic reconstruction carried out on taxonprint data demonstrated that this approach could be of general utility for molecular systematics and species identification. Received: 12 January 1998 / Accepted: 16 May 1998     

Cladistic analysis of molecular and morphological data

Considerable progress has been made recently in phylogenetic reconstruction in a number of groups of organisms. This progress coincides with two major advances in systematics: new sources have been found for potentially informative characters (i. e., molecular data) and (more importantly) new approaches have been developed for extracting historical information from old or new characters (i. e., Hennigian phylogenetic systematics or cladistics). The basic assumptions of cladistics (the existence and splitting of lineages marked by discrete, heritable, and independent characters, transformation of which occurs at a rate slower than divergence of lineages) are discussed and defended. Molecular characters are potentially greater in quantity than (and usually independent of) more traditional morphological characters, yet their great simplicity (i. e., fewer potential character states; problems with determining homology), and difficulty of sufficient sampling (particularly from fossils) can lead to special difficulties. Expectations of the phylogenetic behavior of different types of data are investigated from a theoretical standpoint, based primarily on variation in the central parameter λ (branch length in terms of expected number of character changes per segment of a tree), which also leads to possibilities for character and character state weighting. Also considered are prospects for representing diverse yet clearly monophyletic clades in larger-scale cladistic analyses, e. g., the exemplar method vs. “compartmentalization” (a new approach involving substituting an inferred “archetype” for a large clade accepted as monophyletic based on previous analyses). It is concluded that parsimony is to be preferred for synthetic, “total evidence” analyses because it appears to be a robust method, is applicable to all types of data, and has an explicit and interpretable evolutionary basis. © 1994 Wiley-Liss, Inc.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

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.     

Evolutionary theory and systematics: relationships between process and patterns

The relevance of the Modern Evolutionary Synthesis to the foundations of taxonomy (the construction of groups, both taxa and phyla) is reexamined. The nondimensional biological species concept, and not the multidimensional, taxonomic, species notion which is based on it, represents a culmination of an evolutionary understanding. It demonstrates how established evolutionary mechanisms acting on populations of sexually reproducing organisms provide the testable ontological basis of the species category. We question the ontology and epistemology of the phylogenetic or evolutionary species concept, and find it to be a fundamentally untenable one. We argue that at best, the phylogenetic species is a taxonomic species notion which is not a theoretical concept, and therefore should not serve as foundation for taxonomic theory in general, phylogenetics, and macroevolutionary reconstruction in particular. Although both evolutionary systematists and cladists are phylogeneticists, the reconstruction of the history of life is fundamentally different in these two approaches. We maintain that all method, including taxonomic ones, must fall out of well corroborated theory. In the case of taxonomic methodology the theoretical base must be evolutionary. The axiomatic assumptions that all phena, living and fossil, must be holophyletic taxa (species, and above), resulting from splitting events, and subsequently that evaluation of evolutionary change must be based on a taxic perspective codified by the Hennig ian taxonomic species notion, are not testable premises. We discuss the relationship between some biologically, and therefore taxonomically, significant patterns in nature, and the process dependence of these patterns. Process-free establishment of deductively tested “genealogies” is a contradiction in terms; it is impossible to “recover” phylogenetic patterns without the investment of causal and processual explanations of characters to establish well tested taxonomic properties of these (such as homologies, apomorphies, synapomorphies, or transformation series). Phylogenies of either characters or of taxa are historical-narrative explanations (H-N Es), based on both inductively formulated hypotheses and tested against objective, empirical evidence. We further discuss why construction of a “genealogy”, the alleged framework for “evolutionary reconstruction”, based on a taxic, cladistic outgroup comparison and a posteriori weighting of characters is circular. We define how the procedure called null-group comparison leads to the noncircular testing of the taxonomic properties of characters against which the group phylogenies must be tested. This is the only valid rooting procedure for either character or taxon evolution. While the Hennig -principle is obviously a sound deduction from the theory of descent, cladistic reconstruction of evolutionary history itself lacks a valid methodology for testing transformation hypotheses of both characters and species. We discuss why the paleontological method is part of comparative biology with a critical time dimension ana why we believe that an “ontogenetic method” is not valid. In our view, a merger of exclusive (causal and interactive, but best described as levels of organization) and inclusive (classificatory) hierarchies has not been accomplished by a taxic scheme of evolution advocated by some. Transformational change by its very nature is not classifiable in an inclusive hierarchy, and therefore no classification can fully reflect the causal and interactive chains of events constituting phylogeny, without ignoring and contradicting large areas of corroborated evolutionary theory. Attempts to equate progressive evolutionary change with taxic schemes by Haeckel were fundamentally flawed. His ideas found 19th century expression in a taxic perception of the evolutionary process (“phylogenesis”), a merger of typology, hierarchic and taxic notions of progress, all rooted in an ontogenetic view of phylogeny. The modern schemes of genealogical hierarchies, based on punctuation and a notion of “species” individuality, have yet to demonstrate that they hold promise beyond the Haeckel ian view of progressive evolution.     

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.     

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.     

Stability, sensitivity, science and heurism

We examine recently proposed justifications of sensitivity analysis sensu Wheeler (1995 ), here referred to as weighted‐classes sensitivity analysis (WCSA). We refute Giribet's (2003a) claim that WCSA is the strictest possible test for a given phylogenetic hypothesis. Giribet's (2003a) classification of data exploration methods as evaluating “nodal stability” or “nodal support” is arbitrary, at odds with common usage and actually obscures the relationships between the methods he examined, all of which seek to assess the sensitivity of results to variation in analytical conditions. Stability, whether statistical or taxonomic, is not a goal of phylogenetic science. Statistical stability necessarily involves trial repetition, which is impossible in ideographic sciences like phylogenetics. Taxonomic stability can be nothing more than an unintended by‐product of scientific inquiry, i.e., the repeated failure to refute a hypothesis. Schulmeister's (2003 ) “robust‐choice” defense of WCSA does not succeed in placing non‐arbitrary bounds on parameters, and her interpretation of this approach as simultaneously verificationist and falsificationist is logically inconsistent. WCSA is neither scientific nor heuristic and therefore does not contribute to the advancement of objective knowledge claims. © The Willi Hennig Society 2005.     

Extended phylogeny of the Craspedida (Choanomonada)

Currently choanoflagellates are classified into two distinct orders: loricate Acanthoecida and non-loricate Craspedida. The morphologically based taxonomy of the order Craspedida is in need of a revision due to its controversial, paraphyletic and inconsistent systematics and nomenclature. In this study, we add molecular data (SSU and parts of the LSU rDNA) of six new Craspedida species isolated from saline, brackish and freshwater habitats to the existing knowledge. Four of these six organisms could be described as new species: Paramonosiga thecata, “Salpingoeca” euryoecia, “Salpingoeca” ventriosa, “Sphaeroeca” leprechaunica, whereas two are assigned to previous morphologically described species: “Salpingoeca” fusiformis Saville Kent, 1880 and “Salpingoeca” longipes Saville Kent, 1880. Paramonosiga is established as a new genus of the Craspedida based on its phylogenetic position. Extending the dataset by six additional sequences shows that the craspedid taxonomy is still unsolved as the type specimen Salpingoeca gracilis has not yet been sequenced and hence a clear assignment to the genus Salpingoeca is not possible. Trying to assign morphological and ecological data to phylogenetic clades is not successful. We give an improved/emended morphological diagnosis for the two redescribed species and add molecular data for all six species, shedding light on their phylogenetic position.     

Willi Hennig’s dichotomization of nature

Two formal assumptions implied in Willi Hennig’s “phylogenetic systematics” were repeatedly criticized for not being biologically grounded. The first is that speciation is always dichotomous; the second is that the stem‐species always goes extinct when its lineage splits into two daughter species. This paper traces the theoretical roots of Hennig’s “principle of dichotomy”. While often considered merely a methodological principle, Hennig’s realist perspective required him to ground the “principle of dichotomy” ontologically in speciation. As a methodological principle, the adherence to a strictly dichotomously structured phylogenetic system allowed Hennig to be unequivocal in character analysis and precise in the rendition of phylogenetic relationships. The ontological grounding of the “principle of dichotomy” in speciation remains controversial, however. This has implications for the application of techniques of phylogeny reconstruction to populations of bisexually reproducing organisms (phylogeography). Beyond that, the “principle of dichotomy” has triggered an intensive debate with respect to phylogeny reconstruction at the prokaryote level. © The Willi Hennig Society 2010.     

Paraphyly,ancestors, and the goals of taxonomy: A botanical defense of cladism

Cronquist (1987) criticizes cladism for its rejection of paraphyletic groups, which he would retain if he feels they are “conceptually useful.” We argue that paraphyletic higher taxa are artificial classes created by taxonomists who wish to emphasize particular characters or phenetic “gaps,” and that formal recognition of such taxa conveys a misleading picture of common ancestry and character evolution. In our view, classifications should accurately reflect the nested hierarchy of monophyletic groups that is the natural outcome of the evolutionary process. Such systems facilitate the study of evolution and provide an efficient summary of character distributions. Paraphyletic groups, such as “prokaryotes,” “green algae,” “bryophytes,” and “gymnosperms,” should be abandoned, as continued recognition of such groups will only serve to retard progress in understanding evolution. Contrary to Cronquist’s (1987) assertions, cladistic theory is not at odds with standard views on speciation and the existence of ancestors. Groups of interbreeding organisms can continue to exist after giving rise to descendant species, and there are several ways in which such groups, whether extant or extinct, can be incorporated into cladistic classification. In contrast, paraphyletic higher taxa are neither cohesive (integrated by gene flow) nor whole, do not serve as ancestors, and are unacceptable in the phylogenetic system. Fossils may be of great value in assessing phylogenetic relationships and are readily accommodated in cladistic classification. Cladistic studies are helping to answer major questions about plant evolution, and we anticipate increased efforts to develop a truly phylogenetic system.     

A phylogenetic approach to cultural evolution

There has been a rapid increase in the use of phylogenetic methods to study the evolution of languages and culture. Languages fit a tree model of evolution well, at least in their basic vocabulary, challenging the view that blending, or admixture among neighbouring groups, was predominant in cultural history. Here, we argue that we can use language trees to test hypotheses about not only cultural history and diversification, but also bio-cultural adaptation. Phylogenetic comparative methods take account of the non-independence of cultures (Galton's problem), which can cause spurious statistical associations in comparative analyses. Advances in phylogenetic methods offer new possibilities for the analysis of cultural evolution, including estimating the rate of evolution and the direction of coevolutionary change of traits on the tree. They also enable phylogenetic uncertainty to be incorporated into the analyses, so that one does not have to treat phylogenetic trees as if they were known without error.     

CHARACTER DEFINITIONS AND CHARACTER STATE DELINEATION: THE BETE NOIRE OF PHYLOGENETIC INFERENCE

Abstract— Currently characters are static concepts whose definition and state delineations seldom undergo any scrutiny. Common systematic practice tends to synthesize character slates by combining or dividing observed conditions, a situation most likely due to current theoretical limitations in phylogenetic inference, which tends to ignore problems of multistate characters. This process we refer to as the “synthetic” method for character definition. Character definitions derived for the genera of North American Cochylini (Lepidoptera: Tortricidae) using “synthetic” character states postulated that the cochylines were not monophyletic. The use of cladogram characters and nearest neighbor matrices in uncovering potential flaws in character state delineation is demonstrated. The “synthetic” set of character definitions proved deficient upon such analysis, principally due to its attempt to force highly variable features into a few states. The set of character definitions produced from this analysis is referred to as “reflective” because it does not ignore observed variation. It produces characters with many states and presents problems of setting up transformation series. Three means lor deriving transformations are applied to produce transformation series for the reflective set of character definitions: the unordered outgroup method, morphocline analysis and Transformation Series Analysis (TSA). All three data sets postulated the Cochylini as monophyletic. The three sets of phylogenies were compared. Consensus trees are ambiguous when analysing changes in hierarchy. In order to summarize these results in a manner which does not destroy the phylogenetic structure, positional subtrees, a new means for summarizing multiple solution cladograms, are introduced. It was found that all three sets of transformations produced very different cladograms which in turn were very different from the tree produced by the original, synthetic definitions. The results of each of these methods were assessed for their internal consistency. TSA gave the least contradictory results.     

Reflections on Systematics and Phylogenetic Reconstruction

I attempt to raise questions regarding elements of systematics—primarily in the realm of phylogenetic reconstruction—in order to provoke discussion on the current state of affairs in this discipline, and also evolutionary biology in general: e.g., conceptions of homology and homoplasy, hypothesis testing, the nature of and objections to Hennigian “phylogenetic systematics”, and the schism between (neo)Darwinian descendants of the “modern evolutionary synthesis” and their supposed antagonists, cladists and punctuationalists.     

IS A NEW AND GENERAL THEORY OF MOLECULAR SYSTEMATICS EMERGING?

The advent and maturation of algorithms for estimating species trees—phylogenetic trees that allow gene tree heterogeneity and whose tips represent lineages, populations and species, as opposed to genes—represent an exciting confluence of phylogenetics, phylogeography, and population genetics, and ushers in a new generation of concepts and challenges for the molecular systematist. In this essay I argue that to better deal with the large multilocus datasets brought on by phylogenomics, and to better align the fields of phylogeography and phylogenetics, we should embrace the primacy of species trees, not only as a new and useful practical tool for systematics, but also as a long‐standing conceptual goal of systematics that, largely due to the lack of appropriate computational tools, has been eclipsed in the past few decades. I suggest that phylogenies as gene trees are a “local optimum” for systematics, and review recent advances that will bring us to the broader optimum inherent in species trees. In addition to adopting new methods of phylogenetic analysis (and ideally reserving the term “phylogeny” for species trees rather than gene trees), the new paradigm suggests shifts in a number of practices, such as sampling data to maximize not only the number of accumulated sites but also the number of independently segregating genes; routinely using coalescent or other models in computer simulations to allow gene tree heterogeneity; and understanding better the role of concatenation in influencing topologies and confidence in phylogenies. By building on the foundation laid by concepts of gene trees and coalescent theory, and by taking cues from recent trends in multilocus phylogeography, molecular systematics stands to be enriched. Many of the challenges and lessons learned for estimating gene trees will carry over to the challenge of estimating species trees, although adopting the species tree paradigm will clarify many issues (such as the nature of polytomies and the star tree paradox), raise conceptually new challenges, or provide new answers to old questions.