A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns

Journal name:
Nature
Volume:
468,
Pages:
815–818
Date published:
DOI:
doi:10.1038/nature09632
Received
Accepted
Published online

Parallels between phylogeny and ontogeny have been discussed for almost two centuries, and a number of theories have been proposed to explain such patterns1. Especially elusive is the phylotypic stage, a phase during development where species within a phylum are particularly similar to each other2, 3, 4, 5, 6. Although this has formerly been interpreted as a recapitulation of phylogeny1, it is now thought to reflect an ontogenetic progression phase2, where strong constraints on developmental regulation and gene interactions exist2, 3. Several studies have shown that genes expressed during this stage evolve at a slower rate, but it has so far not been possible to derive an unequivocal molecular signature associated with this stage7, 8, 9, 10, 11, 12, 13, 14, 15. Here we use a combination of phylostratigraphy16 and stage-specific gene expression data to generate a cumulative index that reflects the evolutionary age of the transcriptome at given ontogenetic stages. Using zebrafish ontogeny and adult development as a model, we find that the phylotypic stage does indeed express the oldest transcriptome set and that younger sets are expressed during early and late development, thus faithfully mirroring the hourglass model of morphological divergence2, 3. Reproductively active animals show the youngest transcriptome, with major differences between males and females. Notably, ageing animals express increasingly older genes. Comparisons with similar data sets from flies and nematodes show that this pattern occurs across phyla. Our results indicate that an old transcriptome marks the phylotypic phase and that phylogenetic differences at other ontogenetic stages correlate with the expression of newly evolved genes.

At a glance

Figures

  1. Transcriptome age profiles for the zebrafish ontogeny.
    Figure 1: Transcriptome age profiles for the zebrafish ontogeny.

    a, Cumulative transcriptome age index (TAI) for the different developmental stages. The pink shaded area represents the presumptive phylotypic phase in vertebrates. The overall pattern is significant by repeated measures ANOVA (P = 2.4×10−15, after Greenhouse–Geisser correction P = 0.024). Grey shaded areas represent±the standard error of TAI estimated by bootstrap analysis. b, Transcriptome indices split according to the origin of the genes from the different phylostrata, based on the same developmental series as in a. c, Depiction of the phylostrata analysed; numbers in parentheses denote the number of array probes analysed for each phylostratum.

  2. Relative expression of the genes from each phylostratum across the zebrafish ontogeny (same stages as in Fig. 1) for selected phylostrata with significant differences.
    Figure 2: Relative expression of the genes from each phylostratum across the zebrafish ontogeny (same stages as in Fig. 1) for selected phylostrata with significant differences.

    See Supplementary Fig. 3 for representation of all phylostrata and significance assessments. For easier comparisons, the relative expression calculated in relation to the highest (0) and lowest (1) expression values across developmental stages is shown (see Methods). Bl, blastula; Cl, cleavage; G, gastrula; H, hatching; Juv, juvenile; Ph, pharyngula; Se, segmentation; Z, zygote.

  3. Transcriptome age profiles for the Drosophila ontogeny, based on the data in ref. 23.
    Figure 3: Transcriptome age profiles for the Drosophila ontogeny, based on the data in ref. 23.

    a, Cumulative transcriptome index for the different developmental stages. The pink shaded area represents the presumptive phylotypic phase in insects. The overall pattern of differences in TAI is significant by repeated measures ANOVA (P = 2.5×10−93, after Greenhouse–Geisser correction P = 1.22 × 10−11). Grey shaded areas represent±the standard error of TAI estimated by bootstrap analysis. b, c Same as for Fig. 1b, c.

  4. Comparison of differences in TAI between females and males.
    Figure 4: Comparison of differences in TAI between females and males.

    Comparison across phylostrata in zebrafish (Danio) and Drosophila (see Supplementary Fig. 4 for a plot that includes the differences between stages). The grey shaded area designates the shared part of the phylogeny between the two species (origin of the first cell until the last common ancestor of Bilateria, ps1–ps7). Note that the ps14 value for Drosophila is off the scale (difference is given in parenthesis).

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Primary accessions

Gene Expression Omnibus

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Affiliations

  1. Max-Planck-Institut für Evolutionsbiologie, August-Thienemannstrasse 2, 24306 Plön, Germany

    • Tomislav Domazet-Lošo &
    • Diethard Tautz
  2. Laboratory of Evolutionary Genetics, Division of Molecular Biology, Ruđer Bošković Institute, Bijenička cesta 54, P.P. 180, 10002 Zagreb, Croatia

    • Tomislav Domazet-Lošo

Contributions

T.D.-L. conceived the basic idea and conducted the experiments; D.T. contributed to the evaluation and interpretation of the results. Both authors wrote the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Themicroarray data for zebrafishwere depositedat theNCBIGene Expression Omnibus (GEO) repository under the accession number GSE24616.

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  1. Supplementary Information (1.9M)

    This file contains Supplementary Notes 1- 2, additional references and Supplementary Figures 1- 4 with legends.

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