A priori assumptions about characters as a cause of incongruence between molecular and morphological hypotheses of primate interrelationships

When molecules and morphology produce incongruent hypotheses of primate interrelationships, the data are typically viewed as incompatible, and molecular hypotheses are often considered to be better indicators of phylogenetic history. However, it has been demonstrated that the choice of which taxa to include in cladistic analysis as well as assumptions about character weighting, character state transformation order, and outgroup choice all influence hypotheses of relationships and may positively influence tree topology, so that relationships between extant taxa are consistent with those found using molecular data. Thus, the source of incongruence between morphological and molecular trees may lie not in the morphological data themselves but in assumptions surrounding the ways characters evolve and their impact on cladistic analysis. In this study, we investigate the role that assumptions about character polarity and transformation order play in creating incongruence between primate phylogenies based on morphological data and those supported by multiple lines of molecular data. By releasing constraints imposed on published morphological analyses of primates from disparate clades and subjecting those data to parsimony analysis, we test the hypothesis that incongruence between morphology and molecules results from inherent flaws in morphological data. To quantify the difference between incongruent trees, we introduce a new method called branch slide distance (BSD). BSD mitigates many of the limitations attributed to other tree comparison methods, thus allowing for a more accurate measure of topological similarity. We find that releasing a priori constraints on character behavior often produces trees that are consistent with molecular trees. Case studies are presented that illustrate how congruence between molecules and unconstrained morphological data may provide insight into issues of polarity, transformation order, homology, and homoplasy.     

The role of ontogeny in wood diversity and evolution

Evolutionary developmental biology (evo-devo) explores the link between developmental patterning and phenotypic change through evolutionary time. In this review, we highlight the scientific advancements in understanding xylem evolution afforded by the evo-devo approach, opportunities for further engagement, and future research directions for the field. We review evidence that (1) heterochrony—the change in rate and timing of developmental events, (2) homeosis—the ontogenetic replacement of features, (3) heterometry—the change in quantity of a feature, (4) exaptation—the co-opting and repurposing of an ancestral feature, (5) the interplay between developmental and capacity constraints, and (6) novelty—the emergence of a novel feature, have all contributed to generating the diversity of woods. We present opportunities for future research engagement, which combine wood ontogeny within the context of robust phylogenetic hypotheses, and molecular biology.     

Heterochrony revisited: the evolution of developmental sequences

The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.     

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.     

Anuran limbs reflect microhabitat and distal,later-developing bones are more evolutionarily labile*

Tetrapod limbs have been used as a model system to investigate how selective pressures and constraints shape morphological evolution. Anurans have had many independent transitions to various microhabitats, allowing us to dissect how these factors influence limb morphology. Furthermore, anurans provide a unique system to test the generality of developmental constraints proposed in mammals, namely that later-developing limb bones are under less constraint and show more variation. We used microcomputed tomography scans of 236 species from 52 of 55 families, geometric morphometrics, and modern phylogenetic comparative methods to examine how limb bones are related to microhabitat, phylogeny, allometry, and developmental timing. Although there was significant phylogenetic signal, anuran limb shape showed a relationship with microhabitat and to a lesser extent, body size. We found that distal bones had higher evolutionary rates than proximal bones, providing evidence that developmental constraints are reduced in later-developing bones. Distal bones also showed increased selection related to allometry and microhabitat, providing an additional explanation for higher evolutionary rates. By looking at the evolution of limb shape across a diverse clade, we demonstrated that multiple factors have shaped anuran limbs and that greater evolutionary lability in later-developing limb bones is likely a general trend among tetrapods.     

Reanalysis of oviposition and development rates in the Phytoseiidae using a phylogenetic autoregressive method

Life history patterns are usually identified by comparisons of extant species. Because of inferences regarding phylogenetic constraints, comparative data are often not statistically independent. In order to remove phylogenetic patterns embedded in life history data completely, we adopted a phylogenetic autoregressive method to reanalyse a data set of the ovipositional and developmental rates of 45 Phytoseiidae species. We first calculated the phylogenetic correlation in relation to different taxonomic levels using Moran's I statistics. Significant and positive phylogenetic correlations were found at the subgenus and subfamily levels. This indicates that some variation in both of these life-history traits could be accounted for by phylogeny. Phylogenetic associations, therefore, were removed by a phylogenetic autoregressive method. Using corrected data from this method, the specific components of the ovipositional rate are positively correlated with the specific components of th e developmental rate. The method that we have used obtains the same conclusion as others but differs from the phylogenetic effect in the way that it influences the relationship between comparative data. Because of no data reduction in the phylogenetic autoregressive method, the specific components are more useful than the mean values derived from the higher taxonomic nodes for testing ecological and evolutionary hypotheses about life history patterns. © Rapid Science Ltd. 1998     

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time

Convergent evolution is a central concept in evolutionary theory but the underlying mechanism has been largely debated since On the Origin of Species. Previous hypotheses predict that developmental constraints make some morphologies more likely to arise than others and natural selection discards those of the lowest fitness. However, the quantification of the role and strength of natural selection and developmental constraint in shaping convergent phenotypes on macroevolutionary timescales is challenging because the information regarding performance and development is not directly available. Accordingly, current knowledge of how embryonic development and natural selection drive phenotypic evolution in vertebrates has been extended from studies performed at short temporal scales. We propose here the organization of the tetrapod body-axis as a model system to investigate the developmental origins of convergent evolution over hundreds of millions of years. The quantification of the primary developmental mechanisms driving body-axis organization (i.e. somitogenesis, homeotic effects and differential growth) can be inferred from vertebral counts, and recent techniques of three-dimensional computational biomechanics have the necessary potential to reveal organismal performance even in fossil forms. The combination of both approaches offers a novel and robust methodological framework to test competing hypotheses on the functional and developmental drivers of phenotypic evolution and evolutionary convergence.     

EVOLUTION AND MORPHOGENETIC RULES: THE SHAPE OF THE VERTEBRATE LIMB IN ONTOGENY AND PHYLOGENY

The notion of a “developmental constraint” has become a catchphrase for a collection of poorly defined notions about how ontogeny affects phylogeny. In this paper, we shall attempt to define this idea more precisely by examining the vertebrate limb from three viewpoints. First, theoretical models of morphogenesis suggest several generalizations about how limb geometry is laid down during development. Comparative studies and experimental manipulations of developing limbs independently confirm these generalizations, which amount to a set of “construction rules” for determining how the major features of limb architecture are established in ontogeny. Armed with these rules, we can inquire how limb morphology can be varied during evolution and suggest a more precise operational definition of “developmental constraints” on morphological evolution.     

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.     

Metamorphosis of the loop in Cenozoic dallinacean brachiopods and its developmental constraint

Gunji, Yukio 1987 07 15: Metamorphosis of the loop in Cenozoic dallinacean brachiopods and its developmental constraint.
The well-known metamorphosis of loop development in select species of Dallinacea is investigated by numerical analysis. It is shown how loop transformation depends on the location of the 'loop center', that stage forms are determined by the position of the center, and that there may be two 'shift directions'. The succession found in Campages, Laqueur and Dallina can be explained by a posterior shift, while the succession found in Terebratalia and Coptothyris is explained by an anterior shift. These two directions may be linked, because both are found in a single species Nipponithyris afra. Loop development in species of Dallinacea can therefore be transformed through variation of a specific constraint; this is regarded as an example of developmental constraint. Developmental constraints as common features are useful in studying comparative morphology during ontogeny and phylogeny.     

Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies

Evolution can be viewed as a series of changes in the developmental program along the phylogenetic tree. To better understand the early evolution of the vertebrate skull, we can use the embryos of the cyclostome species as models. By comparing the cyclostome developmental patterns with those of gnathostomes, it becomes possible to distinguish the primitive and derived parts of the developmental program as taxon-specific traits. These traits are often recognizable as developmental constraints that define taxa by biasing the developmental trajectories within a certain limited range, resulting in morphological homologies in adults. These developmental constraints are distributed on the phylogenetic tree like the morphological character states of adult animals and are associated with specific regions of the tree. From this perspective, we emphasize the importance of considering gene expression and embryonic anatomy as the mechanistic bases that can result in homologous or nonhomologous morphological patterns at later developmental stages. Taking the acquisition of the jaw and trabecula cranii as examples, we demonstrate that a set of embryonic features can be coupled or decoupled during evolution and development. When they are coupled, they exert an ancestral developmental constraint that results in homologous morphological patterns, and when they are decoupled, the ancestral constraints tend to be abandoned, generating a new body plan. The heterotopy behind the specification of the oral domain is an example of decoupling, based on shifted tissue interactions. We also stress the importance of "developmental burden" in determining the sequential order of changes through evolution.     

THE DIVERSITY AND EVOLUTION OF BATESIAN MIMICRY IN PAPILIO SWALLOWTAIL BUTTERFLIES

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio , and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.     

Determining the role that ecological and developmental constraints play in controlling disparity: examples from the crinoid and blastozoan fossil record

It is widely believed that morphological constraints are responsible for the observed pattern of decreasing major morphological innovation in both the Metazoa and Metaphytes over geological time. This is readily seen as the decreasing trend of origination of higher taxa: phyla, classes, and orders. Currently, there are two competing evolutionary hypotheses that have been proposed to explain this phenomenon: (1) the empty ecospace hypothesis and (2) the developmental constraint hypothesis. To distinguish between hypotheses 1 and 2, the change of morphological innovation before and after several mass extinction events was measured in the Crinoidea and Blastozoa. Mass extinction intervals provided a means in which to remove ecospace limiting constraints and allow the developmental constraint hypothesis to be thoroughly tested. Within the Crinoidea, disparity was measured before and after three mass extinctions. Within the Blastozoa, disparity was measured before and after two mass extinctions. For each taxon, three suites of characters were analyzed: ecological, nonecological, or "developmental" and a combination of the two previous suites plus 50 additional characters. Four different measures of disparity were used to analyze each character suite. In the majority of the cases investigated, disparity rebounds to comparable levels or in some cases higher levels in both the Crinoidea and Blastozoa. The results indicate that developmental constraints are not responsible for the decrease in disparity throughout the geologic range of the taxa. The more likely scenario is that increasingly structured ecological guilds have made it much more difficult to allow large increases in disparity.     

A phylogeny of the Platyhelminthes: towards a total-evidence solution

We advocate a total-evidence approach for the reconstruction of working phylogenies for the Turbellaria and the phylum Platyhelminthes. Few morphology-based character matrices are available in the systematic literature concerning flatworms, and molecular-based phylogenies are rapidly providing the only means by which we can estimate phylogenies cladistically. Character matrices based on gross morphology and ultrastructure are required and should be internally consistent, i.e. character coding should follow a set of a priori guidelines and character duplication and contradiction is avoided. In order to test our molecular phylogenies we need complementary data sets from morphology. To understand morphological homology we need phylogenetic evidence from independent (e.g. molecular) data. Fully complementary morphological and molecular data sets enable us to validate phylogenetic hypotheses and the combination of these sets in phylogenetic reconstruction utilises all statements of homology. Working phylogenies which include all phylogenetic information not only shed light on individual character evolution, but form a strong basis for comparative studies investigating the origin and evolutionary radiation of the taxonomic group under scrutiny. This revised version was published online in July 2006 with corrections to the Cover Date.     

Enantiomorphs differ in shape in opposite directions between populations

Abstract Development is left–right reversed between dextral and sinistral morphs of snails. In sympatry, they share the same gene pool, including polygenes for shell shape. Nevertheless, their shell shapes are not the mirror images of each other. This triggered a debate between hypotheses that argue either for a developmental constraint or for zygotic pleiotropic effects of the polarity gene. We found that dextrals can be wider or narrower than sinistrals depending on the population, contrary to the prediction of invariable deviation under a developmental constraint. If the pleiotropy is solely responsible instead, the mean shape of each morph should change, depending on the frequency of polarity genotype. Our simulations of this mean shape change under zygotic pleiotropy, however, show that the direction of interchiral difference remains the same regardless of genotype frequency. Our results suggest the presence of genetic variation among populations that changes the maternal or zygotic pleiotropic effect of the polarity gene.     

Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis

Embryogenesis relies on instructions provided by spatially organized signaling molecules known as morphogens. Understanding the principles behind morphogen distribution and how cells interpret locally this information remains a major challenge in developmental biology. Here, we introduce morphogen‐age measurements as a novel approach to test models of morphogen gradient formation. Using a tandem fluorescent timer as a protein age sensor, we find a gradient of increasing age of Bicoid along the anterior–posterior axis in the early Drosophila embryo. Quantitative analysis of the protein age distribution across the embryo reveals that the synthesis–diffusion–degradation model is the most likely model underlying Bicoid gradient formation, and rules out other hypotheses for gradient formation. Moreover, we show that the timer can detect transitions in the dynamics associated with syncytial cellularization. Our results provide new insight into Bicoid gradient formation and demonstrate how morphogen‐age information can complement knowledge about movement, abundance, and distribution, which should be widely applicable to other systems.     

PASOS: a method for the phylogenetic analysis of shape ontogenies

We present a novel phylogenetic approach to infer ancestral ontogenies of shape characters described as landmark configurations. The method is rooted in previously published theoretical developments to analyse landmark data in a phylogenetic context with parsimony as the optimality criterion, in this case using the minimization of differences in landmark position to define not only ancestral shapes but also the changes in developmental timing between ancestor–descendant shape ontogenies. Evolutionary changes along the tree represent changes in relative developmental timing between ontogenetic trajectories (possible heterochronic events) and changes in shape within each stage. The method requires the user to determine the shape of the specimens between two standard events, for instance birth and onset of sexual maturity. Once the ontogenetic trajectory is discretized into a series of consecutive stages, the method enables the user to identify changes in developmental timing associated with changes in the offset and/or onset of the shape ontogenetic trajectories. The method is implemented in a C language program called SPASOS. The analysis of two empirical examples (anurans and felids) using this novel method yielded results in agreement with previous hypotheses about shape evolution in these groups based on non-phylogenetic analyses.     

Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves

The structure of compound leaves provides flexibility for morphological change by variation in the shapes, sizes and arrangement of leaflets. Here, we conduct a multilevel analysis of shape variation in compound leaves to explore the developmental plasticity and evolutionary potential that are the basis of diversification in leaf shape. We use the methods of geometric morphometrics to study the shapes of individual leaflets and whole leaves in 20 taxa of Potentilla (sensu lato). A newly developed test based on the bootstrap approach suggests that uncertainty in the molecular phylogeny precludes firm conclusions whether there is a phylogenetic signal in the data on leaf shape. For variation among taxa, variation within taxa, as well as fluctuating asymmetry, there is evidence of strong morphological integration. The patterns of variation are similar across all three levels, suggesting that integration within taxa may act as a constraint on evolutionary change.     

Reciprocal illumination in the gene content tree of life

Phylogenies based on gene content rely on statements of primary homology to characterize gene presence or absence. These statements (hypotheses) are usually determined by techniques based on threshold similarity or distance measurements between genes. This fundamental but problematic step can be examined by evaluating each homology hypothesis by the extent to which it is corroborated by the rest of the data. Here we test the effects of varying the stringency for making primary homology statements using a range of similarity (e-value) cutoffs in 166 fully sequenced and annotated genomes spanning the tree of life. By evaluating each resulting data set with tree-based measurements of character consistency and information content, we find a set of homology statements that optimizes overall corroboration. The resulting data set produces well-resolved and well-supported trees of life and greatly ameliorates previously noted inconsistencies such as the misclassification of small genomes. The method presented here, which can be used to test any technique for recognizing primary homology, provides an objective framework for evaluating phylogenetic hypotheses and data sets for the tree of life. It also can serve as a technique for identifying well-corroborated sets of homologous genes for functional genomic applications.