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. 2016 Nov 17;16(1):251.
doi: 10.1186/s12862-016-0825-7.

A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group

Reema Singh  1 , Christina Schilde  1 , Pauline Schaap  2
Affiliations

A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group

Reema Singh et al. BMC Evol Biol. .

Abstract

Background: Dictyostelia are a well-studied group of organisms with colonial multicellularity, which are members of the mostly unicellular Amoebozoa. A phylogeny based on SSU rDNA data subdivided all Dictyostelia into four major groups, but left the position of the root and of six group-intermediate taxa unresolved. Recent phylogenies inferred from 30 or 213 proteins from sequenced genomes, positioned the root between two branches, each containing two major groups, but lacked data to position the group-intermediate taxa. Since the positions of these early diverging taxa are crucial for understanding the evolution of phenotypic complexity in Dictyostelia, we sequenced six representative genomes of early diverging taxa.

Results: We retrieved orthologs of 47 housekeeping proteins with an average size of 890 amino acids from six newly sequenced and eight published genomes of Dictyostelia and unicellular Amoebozoa and inferred phylogenies from single and concatenated protein sequence alignments. Concatenated alignments of all 47 proteins, and four out of five subsets of nine concatenated proteins all produced the same consensus phylogeny with 100% statistical support. Trees inferred from just two out of the 47 proteins, individually reproduced the consensus phylogeny, highlighting that single gene phylogenies will rarely reflect correct species relationships. However, sets of two or three concatenated proteins again reproduced the consensus phylogeny, indicating that a small selection of genes suffices for low cost classification of as yet unincorporated or newly discovered dictyostelid and amoebozoan taxa by gene amplification.

Conclusions: The multi-locus consensus phylogeny shows that groups 1 and 2 are sister clades in branch I, with the group-intermediate taxon D. polycarpum positioned as outgroup to group 2. Branch II consists of groups 3 and 4, with the group-intermediate taxon Polysphondylium violaceum positioned as sister to group 4, and the group-intermediate taxon Dictyostelium polycephalum branching at the base of that whole clade. Given the data, the approximately unbiased test rejects all alternative topologies favoured by SSU rDNA and individual proteins with high statistical support. The test also rejects monophyletic origins for the genera Acytostelium, Polysphondylium and Dictyostelium. The current position of Acytostelium ellipticum in the consensus phylogeny indicates that somatic cells were lost twice in Dictyostelia.

Keywords: Dictyostelia; Evolution of multicellularity; Evolution of soma; Multi-locus phylogeny; Phylogenomics; Taxonomy.

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Figures

Fig. 1
Fig. 1
Bioinformatics pipeline. Chain of procedures for protein selection, cognate gene identification, gene model prediction and phylogenetic analysis
Fig. 2
Fig. 2
Phylogenetic inference from 47 concatenated proteins. a Location of selected species in the previously inferred SSU rDNA phylogeny [10]. b–f Phylogenetic trees inferred by Bayesian inference (b–d), RAxML (e) or Phylobayes (f) from an alignment of 47 concatenated orthologous proteins that were identified in the species shown in a. Bayesian analyses were run for 100,000 generations with either a mixed amino-acid model (b,c) for the entire alignment, or with a partitioned alignment in which each protein was run under its optimal amino-acid substitution model (d). All analyses converged within 6000 generations (SD of split frequencies = 0). The RaxML analysis was run with 100 bootstrap replicates on an alignment partitioned as in d. Phylobayes MPI [22] was run over two chains under the CAT-GTR model (f). Trees were rooted using A. castellani as outgroup. The average GC content of the genomic DNAs encoding the 47 proteins is plotted onto the phylogeny in panel c. Posterior probabilities or bootstrap support for the nodes are shown. Abbreviated and full species names are colour-coded to reflect the taxon group to which the species belong
Fig. 3
Fig. 3
Phylogenetic inference from subsets. The 47 protein set was subdivided in sets of nine or ten proteins by joining the fifth rows of five staggered columns of protein identifiers. The protein alignments were concatenated per set, and each alignment was subjected to Bayesian inference with a mixed amino-acid model. Only set 5 yielded a tree topology that was different (red branch) from the 47 protein consensus topology (top left)
Fig. 4
Fig. 4
Correlations between protein alignment statistics and tree features. For trees inferred from alignments of orthologs for each of the individual 47 test proteins (Additional file 3), the number of non-consensual nodes in each tree was plotted against either the number of aligned (a) or variable (b) positions per alignment, or against the averaged posterior probabilities of all nodes in the tree (c). Averaged posterior probabilities were also plotted against the number of variable positions per alignment (d). Regression lines for all plots are shown with their equations and coefficients of determination. Correlations between the variables were determined by Spearman rank order and P-values are shown. All variables are listed in Additional File 2, sheet 4
Fig. 5
Fig. 5
Alternative tree topologies. Schematic of repositioning of tree branches in the 47 protein consensus tree to yield the most commonly encountered alternative topologies found in either the earlier SSU rDNA tree of Dictyostelia [10], or the trees inferred from single proteins (Additional file 3). All alternative trees are shown in Additional file 5
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