Turning the crown upside down: gene tree parsimony roots the eukaryotic tree of life

Abstract

The first analyses of gene sequence data indicated that the eukaryotic tree of life consisted of a long stem of microbial groups "topped" by a crown-containing plants, animals, and fungi and their microbial relatives. Although more recent multigene concatenated analyses have refined the relationships among the many branches of eukaryotes, the root of the eukaryotic tree of life has remained elusive. Inferring the root of extant eukaryotes is challenging because of the age of the group (∼1.7-2.1 billion years old), tremendous heterogeneity in rates of evolution among lineages, and lack of obvious outgroups for many genes. Here, we reconstruct a rooted phylogeny of extant eukaryotes based on minimizing the number of duplications and losses among a collection of gene trees. This approach does not require outgroup sequences or assumptions of orthology among sequences. We also explore the impact of taxon and gene sampling and assess support for alternative hypotheses for the root. Using 20 gene trees from 84 diverse eukaryotic lineages, this approach recovers robust eukaryotic clades and reveals evidence for a eukaryotic root that lies between the Opisthokonta (animals, fungi and their microbial relatives) and all remaining eukaryotes.

FIGURE 1.

Reconciled tree of eukaryotes reveals a root between Opisthokonta and all remaining eukaryotes. Major clades indicated in colored boxes and nested clades with vertical lines, as described in Table 2. Tree estimated from analysis of 59 taxa in the “15+ out” analysis: taxa found in at least 15 of the 20 genes (Table 1) and including rooted gene trees for the 10 genes with outgroup sequences.

FIGURE 2.

Exemplar single gene tree (HSP90) reveals a topology inconsistent with ultrastructure, previous analyses of multigene data, and with the reconciled tree (Fig. 1). Major clades are not monophyletic but are shaded as in Figure 1 to highlight complexity of single gene trees.