Universal artifacts affect the branching of phylogenetic trees, not universal scaling laws

Abstract

Background: The superficial resemblance of phylogenetic trees to other branching structures allows searching for macroevolutionary patterns. However, such trees are just statistical inferences of particular historical events. Recent meta-analyses report finding regularities in the branching pattern of phylogenetic trees. But is this supported by evidence, or are such regularities just methodological artifacts? If so, is there any signal in a phylogeny?

Methodology: In order to evaluate the impact of polytomies and imbalance on tree shape, the distribution of all binary and polytomic trees of up to 7 taxa was assessed in tree-shape space. The relationship between the proportion of outgroups and the amount of imbalance introduced with them was assessed applying four different tree-building methods to 100 combinations from a set of 10 ingroup and 9 outgroup species, and performing covariance analyses. The relevance of this analysis was explored taking 61 published phylogenies, based on nucleic acid sequences and involving various taxa, taxonomic levels, and tree-building methods.

Principal findings: All methods of phylogenetic inference are quite sensitive to the artifacts introduced by outgroups. However, published phylogenies appear to be subject to a rather effective, albeit rather intuitive control against such artifacts. The data and methods used to build phylogenetic trees are varied, so any meta-analysis is subject to pitfalls due to their uneven intrinsic merits, which translate into artifacts in tree shape. The binary branching pattern is an imposition of methods, and seldom reflects true relationships in intraspecific analyses, yielding artifactual polytomies in short trees. Above the species level, the departure of real trees from simplistic random models is caused at least by two natural factors--uneven speciation and extinction rates; and artifacts such as choice of taxa included in the analysis, and imbalance introduced by outgroups and basal paraphyletic taxa. This artifactual imbalance accounts for tree shape convergence of large trees.

Significance: There is no evidence for any universal scaling in the tree of life. Instead, there is a need for improved methods of tree analysis that can be used to discriminate the noise due to outgroups from the phylogenetic signal within the taxon of interest, and to evaluate realistic models of evolution, correcting the retrospective perspective and explicitly recognizing extinction as a driving force. Artifacts are pervasive, and can only be overcome through understanding the structure and biological meaning of phylogenetic trees. Catalan Abstract in Translation S1.

Figure 1. Distribution of rooted, unlabeled trees in tree-shape space, defined by branch size (A) and cumulative branch size (C).

All trees of up to 7 terminal taxa are shown. Solid symbols indicate binary trees, empty symbols stand for non-binary trees. Ellipses encompass all trees with the same number of terminal taxa (n). The lines are the interpolated expectation for three kinds of trees (the 4-taxa examples shown at right): totally symmetrical, random average (middle); pectinate, most imbalanced (top); and totally unresolved, trivial (bottom). The space actually occupied by all trees is limited by the upper and lower bounds. All binary (fully resolved) trees occur at or above the limit imposed by symmetrical trees. Only trees including at least one polytomy (non-binary, or unresolved) occur below this limit.

Figure 2. Two analyzed phylogenetic trees, redrawn unlabeled and with uniform internodal distances.

A) Fig. 7 from ; B) Fig. 1 from . Ingroup taxa are Arachnida and Pectinidae, respectively. Outgroup taxa are marked by thick vertical lines. Basal non-monophyletic taxa are highlighted.

Figure 3. Relationship between branch size (A) and cumulative branch size (C) throughout two phylogenetic trees (shown in

Fig. 2). Each data point represents a node. Notice the logarithmic scale on both axes. Open circles show data for tree A, solid dots stand for tree B. The diagonal line is the interpolated expectation from a random average, totally symmetrical tree. Arrows point at below-expectation values belonging to multifurcations. The dotted circle encloses rapidly diverging values belonging to outgroup and basal paraphyletic taxa.

Figure 4. Values of log outgroup imbalance plotted against the relative proportion of outgroups in the dataset of trees obtained applying four tree-building methods to 100 combinations of a set of outgroup and ingroup taxa.

Linear regressions are shown for each tree-building method, and for the whole set of 400 trees (thick black line). BA = Bayesian, ML = maximum likelihood, MP = maximum parsimony, NJ = BIONJ distance method.

Figure 5. Values of log outgroup imbalance plotted against the relative proportion of outgroups in the dataset of 61 published phylogenetic trees.

Data points labeled as in Fig. 4.