Syst. Biol. 44(3):281--298, 1995

Thirty Years of Numerical Taxonomy

P. H. A. Sneath

Microbiology and Immunology Department, Leicester University,
Leicester LE1 7RH, England

Abstract.---In this history of numerical taxonomy since the publication in 1963 of Sokal and Sneath's Principles of Numerical Taxonomy, I include reminiscences of the reactions of biologists in Britain and elsewhere. Much of the original program has proved sound. The debate on phenetic and phylogenetic classifications has been valuable, although the logical and theoretical aspects of phenetics have been greatly overlooked in the debate. Hennigian cladistics, however, is a side issue that has not proven its value. Numerical taxonomy in the broad sense is the greatest advance in systematics since Darwin or perhaps since Linnaeus. It has stimulated several new areas of growth, including numerical phylogenetics, molecular taxonomy, morphometrics, and numerical identification. It has wide application outside systematic biology. Landmarks and trends are important aspects of numerical taxonomy. In microbiology, the program of numerical taxonomy has been successful, as indicated by the preponderance of papers describing numerical relationships in the International Journal of Systematic Bacteriology. This review concludes with comments on the needs and prospects of the future. [Numerical taxonomy; phenetics; phylogenetics; cladistics; molecular taxonomy; numerical identification; morphometrics; bacterial systematics.]

Syst. Biol. 44(3):299--320, 1995

Objections to Bootstrapping Phylogenies: A Critique

Michael J. Sanderson1

Department of Biology, University of Nevada,
Reno, Nevada 89557, USA

1 Present address: Section of Evolution and Ecology, University of California,
Davis, California 95616, USA

Abstract.---Despite widespread use, the bootstrap remains a controversial method for assessing confidence limits in phylogenies. Opposition to its use has centered on a small set of basic philosophical and statistical objections that have largely gone unanswered by advocates of statistical approaches to phylogeny reconstruction. The level of generality of these objections varies greatly, however. Some of the objections are merely technical, involving problems that are found in almost all statistical tests, such as bias in small data sets. Other objections are really associated not so much with a rejection of the bootstrap but with the rejection of statistical methods in phylogeny reconstruction, which resurrects an old debate. The most relevant aspects of this debate revolve around the issue of whether or not an unknown parameter, such as a tree, can have probabilities (confidence limits) associated with it. The relevant statistical aspects are reviewed, but because this issue remains controversial within statistical theory, it is unreasonable to expect it to be anything else in phylogenetic systematics. An area of common ground between statistical and nonstatistical approaches emerges in the use of statistical likelihood as a measure of support for phylogenetic hypotheses. This common ground requires the abandonment of classical notions of confidence limits by statistically oriented systematists and the acceptance of probabilistic models and likelihood by opponents of statistical methods. There remains a small set of objections directly germane to bootstrapping phylogenies per se. These objections involve issues of random sampling and whether or not character data are independent and identically distributed (IID). Nonrandom-sample bootstrapping is discussed, as are sample designs that impose the IID assumption on characters regardless of evolutionary nonindependence and nonidentical distribution of those data. Systematists wishing to use the bootstrap have an alternative to making explicit and rather strong evolutionary assumptions; they can consider the issue of character sampling designs much more carefully. [Phylogeny; bootstrap; statistical inference; confidence; cladistics.]

Syst. Biol. 44(3):321--331, 1995

Sequence Alignment, Parameter Sensitivity, and the Phylogenetic Analysis of Molecular Data

Ward C. Wheeler1

Department of Invertebrates, American Museum of Natural History,
Central Park West at 79th Street,
New York, New York 10024-5192, USA

1 E-mail:

Abstract.---The dependence of the results of molecular phylogenetic sequence analysis (both alignment and cladogram construction) on variation in analytical parameters is examined. Phylogenetic analyses of molecular sequence data are necessarily based on intrinsically unmeasurable parameters such as transition--transversion and alignment gap cost ratios (among others). Procedures for robust and liberal hypothesis choice are proposed using congruence as an optimality criterion. To illustrate and explain this process further, data on arthropod relationships are used. The effects of variation in transversion--transition and gap--change ratio parameters on alignment and phylogeny reconstruction are assessed in light of both taxonomic and character-based congruence measures.[Sequence alignment; sensitivity analysis; arthropods; molecular systematics; phylogeny.]

Syst. Biol. 44(3):332--342, 1995

Phylogenetic Noise Leads to Unbalanced Cladistic Tree Reconstructions

Arne O. Mooer1, Roderic D. M. Page, Andy Purvis, and Paul H. Harvey

Department of Zoology, University of Oxford,
South Parks Road, Oxford OX1 3PS, England

1 Present address: Department of Zoology, University of British Columbia,
Vancouver, British Columbia V6T 1Z4, Canada

Abstract.---Cladistic tree balance is the extent to which internal nodes on a cladistic tree define clades of equal size. More robust maximum-parsimony trees taken from the literature are more balanced. Simulation studies suggest that a methodological bias is responsible for this correlation because incorrect reconstructions are also likely to be less balanced than the true trees they estimate. Misinformative cladistic characters can be expected to make trees more unbalanced if there is marked variation in their rates of change. This bias may contribute to the excess of unbalanced phylogenies reported in the literature. [Cladistic tree balance; tree robustness; retention index; homoplasy; Markov models.]

Syst. Biol. 44(3):343--360, 1995

Phylogenetic Analysis of Ontogenetic Shape Transformations: A Reassessment of the Piranha Genus Pygocentrus (Teleostei)

William L. Fink1,3 and Miriam Leah Zelditch2

1 Museum of Zoology and Department of Biology, University of Michigan,
Ann Arbor, Michigan 48109, USA
2 Museum of Paleontology, University of Michigan,
Ann Arbor, Michigan 48109, USA
3 E-mail:

Abstract.---Despite the potential information that may lie in phylogenetic analyses of ontogenies of body form, few studies have examined methods for extracting and analyzing ontogenetic shape characters. We propose and exemplify a procedure for phylogenetic shape analysis. We use the thin-plate spline decomposed by its partial warps, a method that has several critical advantages over available alternatives. Most notably, shape variables extracted by this method refer to localizable features of the morphology. We demonstrate how these characters can be coded and include them in a phylogenetic analysis of the piranha genus Pygocentrus, using a data set also comprising meristic, myological, and osteological characters. Using ontogenies of these localized shape variables, we have corroborated the monophyly of Pygocentrus. Although we found no new characters corroborating the proposed sister-group relationship of P. nattereri and P. cariba, our characters are all congruent with this hypothesis. Several ontogenetic shape characters serve to diagnose the previously undiagnosed P. nattereri. Independence of ontogenetic shape features is assessed in the same manner as for any other features: by examination of their distributions on the corroborated cladogram. In addition to inspecting associations among characters that changed multiple times, character independence was assessed using the information in the kinds of ontogenetic modifications (gain, loss, reorientation, reversal) and the information in observed development. Most of the geometrically independent features extracted during this study are phylogenetically independent of each other. We also found that region-specific ontogenetic allometries are phylogenetically independent of each other. In addition, localized ontogenetic changes along orthogonal body axes (anteroposterior and dorsoventral in this case) are usually phylogenetically independent. Although these findings of character independence may be specific to this study, the method for assessing this independence can be applied generally. Evolution of both spatial and temporal patterns of growth is an inference that depends upon using methods, such as the one employed here, capable of describing the spatial patterning of ontogeny. [Ontogeny; phylogeny; character independence; geometric morphometrics; piranhas; Pygocentrus.]

Syst. Biol. 44(3):361--383, 1995

Feeding, Function, and Phylogeny: Analysis of Historical Biomechanics in Labrid Fishes Using Comparative Methods

Mark W. Westneat1

Center for Evolutionary and Environmental Biology,
Field Museum of Natural History, Chicago, Illinois 60605, USA

1 E-mail:

Abstract.---Recently developed methods in phylogenetic systematics enable the discovery of associations among diverse characters of organisms such as morphology, biomechanics, and ecology among clades. In this study, the results of multiple character correlation techniques were compared using a data set on the functional morphology and ecology of feeding in the Cheilinini and outgroups (Perciformes: Labridae). The following two questions were addressed: What are the patterns of evolutionary change in structure and function of the feeding mechanisms of labrid fishes? Are evolutionary changes in trophic structure, feeding biomechanics, and feeding ecology congruent at different levels of labrid phylogeny? Previous work on the phylogenetic relationships of labrid fishes, quantitative modeling of jaw protrusion and hyoid depression mechanisms, analysis of morphometric variation in the trophic apparatus, and description of the natural diet of labrids was integrated. Analysis of phylogenetic association between dietary and biomechanical characters within the phylogeny was performed using character optimization to map characters onto the phylogeny. Statistical tests of association between pairs of discrete characters involved contingent states tests and concentrated changes tests. Phylogenetic correlations between continuous quantitative characters were determined using the methods of squared-change parsimony, independent contrasts, and phylogenetic autocorrelation. A diversity of techniques yielded similar answers in this case study, suggesting that evolution of dietary habits and feeding behavior is tightly linked to the biomechanics of the feeding apparatus. [Functional morphology; systematics; ecology; character correlation; comparative methods; phylogeny; Labridae.]

Syst. Biol. 44(3):384--399, 1995

Maximum Likelihood Trees from DNA Sequences: A Peculiar Statistical Estimation Problem

Ziheng Yang1,4, Nick Goldman2,5, and Adrian Friday3

1 Department of Zoology, The Natural History Museum,
Cromwell Road, London SW7 5BD, England
2 Laboratory of Mathematical Biology, National Institute for Medical Research,
The Ridgeway, Mill Hill, London NW7 1AA, England
3 Department of Zoology, University of Cambridge,
Downing Street, Cambridge CB2 3EJ, England
4 Present address: Institute of Molecular Evolutionary Genetics,
328 Mueller Laboratory, University Park, Pennsylvania 16802, USA
5 To whom correspondence should be addressed.

Abstract.---The parameter space of the phylogenetic tree estimation problem consists of three components, T, t, and u. The tree topology T is a discrete entity that is not a proper statistical parameter but that can nevertheless be estimated using the maximum likelihood criterion. Its role is to specify the branch length parameters and the form of the likelihood function(s). Branch lengths t are conditional on T and are meaningful only for specific values of T. Parameters ;gu in the model of nucleotide substitution are common to all the tree topologies and represent such values as the transition/transversion rate ratio. T and t thus represent the tree, and u represents the model. With typical DNA sequence data, differences in T have only a small effect on the likelihood, but changing u will influence the likelihood greatly. Estimates of u are also found to be insensitive to T, making it possible to obtain reliable estimates of u and to perform tests concerning the model (u) even if knowledge of the evolutionary relationship (T) is not available. In contrast, tests concerning t, such as testing the existence of a molecular clock, appear to be more difficult to perform when the true topology is unknown. In this paper, we explore the peculiarity of the parameter space of the tree estimation problem and suggest methods for overcoming some difficulties involved with tests concerning the model. We also address difficulties concerning hypothesis testing on T, i.e., evaluation of the reliability of the estimated tree topology. We note that estimation of and particularly tests concerning T depend critically on the assumed model. [Maximum likelihood; models; parameter space; consistency; sampling errors; hypothesis testing; nucleotide substitution; phylogeny estimation; molecular systematics; molecular clock.]

Syst. Biol. 44(3):400--408, 1995

The Biogeography of Sea Islands: Clues from the Population Genetics of the Freshwater Snail, Physa heterostropha

Robert T. Dillon, Jr.1, and Amy R. Wethington2

Department of Biology, College of Charleston,
Charleston, South Carolina 29424, USA

1 E-mail:
2 Present address: Department of Biology, Indiana University,
Jordon Hall 142, Box 42, Bloomington, Indiana 47405, USA

Abstract.---Although entirely surrounded by estuarine waters, the sea islands of South Carolina are of dubious biogeographic integrity. Pleistocene sea level fluctuations have periodically inundated these regions and left them de-watered inland. Samples from 10 populations of the freshwater pulmonate snail, Physa heterostropha, inhabiting six land masses isolated by putative estuarine barriers in the Charleston area were used for allozyme electrophoresis to estimate gene frequencies at 10 polymorphic loci. Although intrapopulation and interpopulation gene diversity was extensive, none of the variance could be attributed to island or land mass by hierarchical analysis of F statistics. The matrix of genetic distances among all sites was significantly correlated with the matrix of linear geographic distances, even though estuaries dissect the study area. Nearest neighbors separated by estuaries tended to be more similar genetically than nearest neighbors sharing a land mass. These data on the population genetics of freshwater snails seem to hold no evidence of biogeographic boundaries among sea islands. Dispersal by birds is a plausible explanation for the observed overall correlation between genetic and geographic distance, but vicariance or natural selection hypotheses cannot be excluded. [Islands; biogeography; isozymes; allozymes; Pulmonata.]

Syst. Biol. 44(3):409--420, 1995

A Phylogenetic Study of the Blackbirds Based on Variation in Mitochondrial DNA Restriction Sites

Scott Freeman1,3 and Robert M. Zink2,4

1 Department of Zoology, NJ-15, University of Washington,
Seattle, Washington 98195, USA
2 Bell Museum, 100 Ecology Building, University of Minnesota,
St. Paul, Minnesota 55108, USA
3 Present address: Burke Museum DB-10, University of Washington,
Seattle, Washington 98195, USA
4 E-mail:

Abstract.---We used a generalized parsimony model to estimate the phylogeny of 47 species in the avian subfamily Icterinae using restriction enzyme cleavage sites in mitochondrial DNA (mtDNA). Deep branches in the tree are poorly resolved, either because blackbirds radiated rapidly after the origin of the clade or because substitutions have saturated sites in the mtDNA. Our tree is similar to one published by Lanyon (1994, Evolution 48:679--693) based on mtDNA sequences, which suggests that lack of basal resolution might be attributable to closely spaced speciation events. Both data sets had similar consistency and retention indices, suggesting comparable information content in these two types of data. Neither the restriction-site tree nor the sequence tree support the monophyly of the genus Agelaius. The restriction-site tree suggests that several traditional taxonomic rearrangements are likely based on phenotypic resemblance rather than phylogeny and that the feature viewed as a key innovation of blackbirds (gaping) might not be the basal condition; gaping might be a composite of characters rather than a single homologous condition. The restriction-site tree suggests that the brood-parasitic cowbird species are not monophyletic, contra the sequence data. A combined analysis of sequences and restriction sites for cowbirds supports the sequence tree of Lanyon (1994); however, we suggest an alternative view of the evolution of brood parasitism that is also consistent with the combined data tree. Polygyny appears to be independently derived within blackbirds. Icterus galbula and I. bullockii, which hybridize and are therefore currently considered a single biological species, are not sister taxa; these are likely phylogenetic species. [Blackbirds; generalized parsimony; maximum likelihood; brood parasitism; mating systems; phylogenetic species concept.]