Steven Poe

The genome of the green anole lizard and a comparative analysis with birds and mammals

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments. Among amniotes, genome sequences are available for mammals and birds, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes. Also, A. carolinensis mobile elements are very young and diverse—more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

Taxon sampling revisited.

Phylogenies that include long, unbranched lineages can be difficult to reconstruct. This is because long-branch taxa (such as rapidly evolving species) may share character states by chance more often than more closely related taxa share derived character states through common ancestry. Despite Kims warning that added taxa can decrease accuracy, some authors have argued that the negative impact of this error, called ‘long-branch attraction’, is minimized when slowly evolving lineages are included to subdivide long branches. From this they have concluded that increasing the number of species sampled per lineage results in better accuracy than increasing the number of characters per species. We find, using computer simulations, that adding characters can be the more favourable strategy, even for long-branched trees, and that adding slowly evolving taxa to subdivide long branches can reduce accuracy.

BIRDS IN A BUSH: FIVE GENES INDICATE EXPLOSIVE EVOLUTION OF AVIAN ORDERS

Abstract All recent studies of bird phylogeny have produced poorly resolved relationships among the orders of Neoaves, the lineage that includes most modern birds. This “bush” result suggests the possibility of an explosive and potentially unresolvable evolutionary radiation. However, simultaneous radiations of multiple lineages are thought to be rare or nonexistent in nature and difficult to corroborate empirically because lack of phylogenetic resolution can also be caused by analytical artifacts. Here we examine the predictions of the explosive radiation hypothesis for five independent genetic datasets for Neoaves. We propose a methodology for testing for polytomies of evolutionary lineages, perform likelihood‐ratio tests to compare trees with zero‐length branches to more resolved trees, compare topologies between independent gene trees, and propose a power test for the SOWH test. The evidence of (1) extremely short (in some cases zero‐length) branches for interordinal relationships across independent gene trees and (2) to‐pological incongruence among gene trees suggests that the bird tree includes essentially simultaneous radiation of multiple lineages. This result explains why a robust phylogeny of birds has not been produced despite much effort on the part of avian systematists.

Philosophy and phylogenetic inference: a comparison of likelihood and parsimony methods in the context of Karl Popper's writings on corroboration.

Advocates of cladistic parsimony methods have invoked the philosophy of Karl Popper in an attempt to argue for the superiority of those methods over phylogenetic methods based on Ronald Fishers statistical principle of likelihood. We argue that the concept of likelihood in general, and its application to problems of phylogenetic inference in particular, are highly compatible with Poppers philosophy. Examination of Poppers writings reveals that his concept of corroboration is, in fact, based on likelihood. Moreover, because probabilistic assumptions are necessary for calculating the probabilities that define Poppers corroboration, likelihood methods of phylogenetic inference--with their explicit probabilistic basis--are easily reconciled with his concept. In contrast, cladistic parsimony methods, at least as described by certain advocates of those methods, are less easily reconciled with Poppers concept of corroboration. If those methods are interpreted as lacking probabilistic assumptions, then they are incompatible with corroboration. Conversely, if parsimony methods are to be considered compatible with corroboration, then they must be interpreted as carrying implicit probabilistic assumptions. Thus, the non-probabilistic interpretation of cladistic parsimony favored by some advocates of those methods is contradicted by an attempt by the same authors to justify parsimony methods in terms of Poppers concept of corroboration. In addition to being compatible with Popperian corroboration, the likelihood approach to phylogenetic inference permits researchers to test the assumptions of their analytical methods (models) in a way that is consistent with Poppers ideas about the provisional nature of background knowledge.

Evaluation of the strategy of long-branch subdivision to improve the accuracy of phylogenetic methods.

Methods for reconstructing evolutionary history are sensitive to the number and position of taxa included in the analysis (e.g., Gauthier et al., 1988; Hendy and Penny, 1989; Lecointre et al., 1993; Poe, 1998). Figure 1 illustrates this phenomenon using parsimony analyses of a sample of four Anolis lizard species from a large matrix of morphological and molecular data (Poe, 2001). Any of the three possible relationships for these species can be obtained by including appropriate additional species in the same analysis. In addition to demonstrating the instability of results relative to taxon sampling, this example shows conclusively that addition of taxa may be beneficial to the accuracy of a phylogenetic analysis but also may be detrimental to accuracy. This conclusion holds because it is possible to change any of the topological results either by adding or by subtracting taxa, and even though we do not know which of these three trees is the true tree, we can assume that one of them is correct and two of them are wrong. One might think that the sensitivity to taxon sampling shown in Figure 1 is restricted to certain methods or to poorly supported trees. Unfortunately this is not the case, as shown in the example in Figure 2. These trees were reconstructed using the mitochondrial DNA sequence data of Jackman et al. (1999) for Anolis lizards. Tree a in Figure 2 is obtained when these taxa are analyzed alone using maximum likelihood and minimum evolution under complex models (HKY + G; Hasegawa et al., 1985; Yang, 1994; parameter values estimated from data) and using parsimony with equal weights for all character changes. Tree b is obtained using these same methods but running the analyses including three other lizard species. This comparison shows that sensitivity to taxon sampling may occur even with strongly supported trees and diverse methods of estimation (and shows that high bootstrap values and strongly supported congruence between methods are not necessarily predictors of accuracy). The above examples show the potentially extreme sensitivity of phylogenetic methods to taxon sampling, but they are of little help in devising a taxon sampling strategy for maximizing the accuracy of a phylogenetic analysis. When a researcher is interested in the relationships of a set of clades from which exemplar taxa are chosen, is it better or worse to include additional taxa in the analysis? Clearly, simply including more taxa without additional character information can be detrimental to accuracy, because more characters are needed to resolve a greater number of nodes. However, addition of more taxa adds information about evolutionary history (e.g., Gauthier et al., 1988), which seems likely to have a positive effect on accuracy. Given these potentially opposing effects, what is the best taxon-sampling strategy for maximizing the accuracy of phylogenetic analyses? Phylogenies that include lineages that have undergone extensive evolution are difficult to reconstruct because of the phenomenon of long branch attraction (Felsenstein, 1978; Huelsenbeck and Hillis, 1993). Thus, a beneficial sampling strategy might involve shortening long branches by including additional taxa, assuming that such taxa exist (Hendy and Penny, 1989). This strategy has been evaluated for the parsimony method by Graybeal (1998) and by Poe and Swofford (1999). Graybeal fulfilled Hendy and Penny’s (1989) prediction that long-branch subdivision can have a strong beneficial effect on the accuracy of estimation of four-taxon trees in the Felsenstein zone of two long opposing branches and a short internal branch. Poe and Swofford (1999) examined a wider range of model trees and discovered several conditions of the kind discussed by Zharkikh and Li (1993) under which long-branch subdivision was detrimental to accuracy. The taxon sampling strategy of long-branch subdivision (LBS) has not been examined for methods other than parsimony. Poe and Swofford (1999) suggested that phylogenetic methods that take branch lengths into account are less likely to be affected by the problems of LBS that afflicted their application of the parsimony method. Pollock and Bruno (2000:1858) concluded that “the notion that added taxa can decrease accuracy . . . should be abandoned as an artifact of parsimony.” Although it seems likely that LBS will be beneficial when the model

Quantitative Tests of General Models for the Evolution of Development

Comparative developmental biologists have proposed models to describe patterns of conserved features in vertebrate ontogeny. The hourglass model suggests evolutionary change is most difficult at an intermediate “phylotypic” stage, the adaptive penetrance model suggests change is easiest at an intermediate stage, and the early conservation model suggests change is easier later in ontogeny. Although versions of some of these models have been discussed since the nineteenth century, quantitative approaches have been proposed only recently. Here we present quantitative phylogenetic approaches to evaluating trends in the evolution of ontogeny. We apply these approaches to the proposed models and demonstrate that an existing approach to assessing these models is biased. We show that the hourglass, adaptive penetrance, and early conservation models are unnecessarily complex explanations of the patterns observed in developmental event data for 14 species of vertebrates. Rather, a simpler model that postulates that evolutionary change is easier between ontogenetically adjacent events is adequate.

Failed Refutations: Further Comments on Parsimony and Likelihood Methods and Their Relationship to Popper's Degree of Corroboration

Kluges (2001, Syst. Biol. 50:322-330) continued arguments that phylogenetic methods based on the statistical principle of likelihood are incompatible with the philosophy of science described by Karl Popper are based on false premises related to Kluges misrepresentations of Poppers philosophy. Contrary to Kluges conjectures, likelihood methods are not inherently verificationist; they do not treat every instance of a hypothesis as confirmation of that hypothesis. The historical nature of phylogeny does not preclude phylogenetic hypotheses from being evaluated using the probability of evidence. The low absolute probabilities of hypotheses are irrelevant to the correct interpretation of Poppers concept termed degree of corroboration, which is defined entirely in terms of relative probabilities. Popper did not advocate minimizing background knowledge; in any case, the background knowledge of both parsimony and likelihood methods consists of the general assumption of descent with modification and additional assumptions that are deterministic, concerning which tree is considered most highly corroborated. Although parsimony methods do not assume (in the sense of entailing) that homoplasy is rare, they do assume (in the sense of requiring to obtain a correct phylogenetic inference) certain things about patterns of homoplasy. Both parsimony and likelihood methods assume (in the sense of implying by the manner in which they operate) various things about evolutionary processes, although violation of those assumptions does not always cause the methods to yield incorrect phylogenetic inferences. Test severity is increased by sampling additional relevant characters rather than by character reanalysis, although either interpretation is compatible with the use of phylogenetic likelihood methods. Neither parsimony nor likelihood methods assess test severity (critical evidence) when used to identify a most highly corroborated tree(s) based on a single method or model and a single body of data; however, both classes of methods can be used to perform severe tests. The assumption of descent with modification is insufficient background knowledge to justify cladistic parsimony as a method for assessing degree of corroboration. Invoking equivalency between parsimony methods and likelihood models that assume no common mechanism emphasizes the necessity of additional assumptions, at least some of which are probabilistic in nature. Incongruent characters do not qualify as falsifiers of phylogenetic hypotheses except under extremely unrealistic evolutionary models; therefore, justifications of parsimony methods as falsificationist based on the idea that they minimize the ad hoc dismissal of falsifiers are questionable. Probabilistic concepts such as degree of corroboration and likelihood provide a more appropriate framework for understanding how phylogenetics conforms with Poppers philosophy of science. Likelihood ratio tests do not assume what is at issue but instead are methods for testing hypotheses according to an accepted standard of statistical significance and for incorporating considerations about test severity. These tests are fundamentally similar to Poppers degree of corroboration in being based on the relationship between the probability of the evidence e in the presence versus absence of the hypothesis h, i.e., between p(e|hb) and p(e|b), where b is the background knowledge. Both parsimony and likelihood methods are inductive in that their inferences (particular trees) contain more information than (and therefore do not follow necessarily from) the observations upon which they are based; however, both are deductive in that their conclusions (tree lengths and likelihoods) follow necessarily from their premises (particular trees, observed character state distributions, and evolutionary models). For these and other reasons, phylogenetic likelihood methods are highly compatible with Karl Poppers philosophy of science and offer several advantages over parsimony methods in this context.

A TEST FOR PATTERNS OF MODULARITY IN SEQUENCES OF DEVELOPMENTAL EVENTS

Abstract This study presents a statistical test for modularity in the context of relative timing of developmental events. The test assesses whether sets of developmental events show special phylogenetic conservation of rank order. The test statistic is the correlation coefficient of developmental ranks of the N events of the hypothesized module across taxa. The null distribution is obtained by taking correlation coefficients for randomly sampled sets of N events. This test was applied to two datasets, including one where phylogenetic information was taken into account. The events of limb development in two frog species were found to behave as a module.

TEST OF VON BAER'S LAW OF THE CONSERVATION OF EARLY DEVELOPMENT

Abstract One of the oldest and most pervasive ideas in comparative embryology is the perceived evolutionary conservation of early ontogeny relative to late ontogeny. Karl Von Baer first noted the similarity of early ontogeny across taxa, and Ernst Haeckel and Charles Darwin gave evolutionary interpretation to this phenomenon. In spite of a resurgence of interest in comparative embryology and the development of mechanistic explanations for Von Baers law, the pattern itself has been largely untested. Here, I use statistical phylogenetic approaches to show that Von Baers law is an unnecessarily complex explanation of the patterns of ontogenetic timing in several clades of vertebrates. Von Baers law suggests a positive correlation between ontogenetic time and amount of evolutionary change. I compare ranked position in ontogeny to frequency of evolutionary change in rank for developmental events and find that these measures are not correlated, thus failing to support Von Baers model. An alternative model that postulates that small changes in ontogenetic rank are evolutionarily easier than large changes is tentatively supported.

Convergent exaptation and adaptation in solitary island lizards

Independent evolutionary lineages often display similar characteristics in comparable environments. Three kinds of historical hypotheses could explain this convergence. The first is adaptive and evolutionary: nonrandom patterns may result from analogous evolutionary responses to shared conditions. The second explanation is exaptive and ecological: species may be filtered by their suitability for a particular type of environment. The third potential explanation is a null hypothesis of random colonization from a historically nonrandom source pool. Here we demonstrate that both exaptation and adaptation have produced convergent similarity in different size-related characters of solitary island lizards. Large sexual size dimorphism results from adaptive response to solitary existence; uniform, intermediate size results from ecological filtering of potential colonizers. These results demonstrate the existence of deterministic exaptive convergence and suggest that convergent phenomena may require historical explanations that are ecological as well as evolutionary.