Dating early animal evolution using phylogenomic data

Abstract

Information about the geological timeframe during which animals radiated into their major subclades is crucial to understanding early animal ecology and evolution. Unfortunately, the pre-Cambrian fossil record is sparse and its interpretation controversial. Relaxed molecular-clock methods provide an alternative means of estimating the timing of cladogenesis deep in the metazoan tree of life. So far, thorough molecular clock studies focusing specifically on Metazoa as a whole have been based on relatively small datasets or incomplete representation of the main non-bilaterian lineages (such as sponges and ctenophores), which are fundamental for understanding early metazoan evolution. Here, we use a previously published phylogenomic dataset that includes a fair sampling of all relevant groups to estimate the timing of early animal evolution with Bayesian relaxed-clock methods. According to our results, all non-bilaterian phyla, as well as total-group Bilateria, evolved in an ancient radiation during a geologically relatively short time span, before the onset of long-term global glaciations ("Snowball Earth"; ~720-635 Ma). Importantly, this result appears robust to alterations of a number of important analytical variables, such as models of among-lineage rate variation and sets of fossil calibrations used.

Figure 1

Age estimates for major animal groups obtained under different molecular clock models. Mean and 95% credibility intervals (CrIs) of age estimates for select nodes obtained with Calibration set A and the 1000 Ma root age prior (see text) under the autocorrelated “ln” (lower bars) and uncorrelated “ugam” (upper bars) relaxed clock models. Taxon names refer to crown groups. “Calc. + Homo.” = Calcarea + Homoscleromorpha clade. Ma = million years before present. Dotted line indicates Precambrian/Cambrian boundary. Gray areas indicate Sturtian (left) and Marinoan (right) glaciations.

Figure 2

Age estimates for major animal groups obtained under different fossil calibration sets. Mean and 95% CrIs of age estimates for select nodes obtained under the autocorrelated “ln” relaxed clock model and the 1000 Ma root age prior using different fossil calibration sets (see text) – A (lower bars), B (middle bars), C (upper bars). Taxon names refer to crown groups. “Calc. + Homo.” = Calcarea + Homoscleromorpha clade. Dotted line indicates Precambrian/Cambrian boundary. Gray areas indicate Sturtian (left) and Marinoan (right) glaciations.

Figure 3

Age estimates for major animal groups obtained under different assumptions about the age of crown-group Opisthokonta. Mean and 95% CrIs of age estimates for select nodes obtained with Calibration set A (see text) under the autocorrelated “ln” relaxed clock model using different root age priors – 1000 ± 100 Ma (lower bars), 1360 ± 100 Ma (middle bars), 800 ± 100 Ma (upper bars). Taxon names refer to crown groups. “Calc. + Homo.” = Calcarea + Homoscleromorpha clade. Dotted line indicates Precambrian/Cambrian boundary. Gray areas indicate Sturtian (left) and Marinoan (right) glaciations.

Figure 4

Time-calibrated phylogeny of animals. Phylogeny of crown-Opisthokonta obtained by Philippe et al., time-calibrated using Calibration set A, an autocorrelated relaxed clock model, and 1000 Ma root age prior (see text). Gray areas indicate Sturtian (left) and Marinoan (right) glaciations. Thick red branches highlight pre-Snowball Earth radiation of animal lineages. Bars at selected deep nodes represent 95% CrIs; above them density plots highlighting the frequency of different age estimates around the mean are shown (produced with custom python and R scripts developed by S. Vargas). Ages in million years before present (Ma). Stratigraphic abbreviations: Ordov., Ordovician; Sil., Silurian; Carbonif., Carboniferous; Pg., Palaeogene; Ng., Neogene. Taxon abbreviations: Hom., Homoscleromorpha; Cal., Calcarea; Hex., Hexactinellida; Dem., Demospongiae; Ant., Anthozoa; Med., Medusozoa; Deut., Deuterostomia; Prot., Protostomia; Ecd., Ecdysozoa; Loph., Lophotrochozoa.