Phylotranscriptomic insights into a Mesoproterozoic-Neoproterozoic origin and early radiation of green seaweeds (Ulvophyceae)

Abstract

The Ulvophyceae, a major group of green algae, is of particular evolutionary interest because of its remarkable morphological and ecological diversity. Its phylogenetic relationships and diversification timeline, however, are still not fully resolved. In this study, using an extensive nuclear gene dataset, we apply coalescent- and concatenation-based approaches to reconstruct the phylogeny of the Ulvophyceae and to explore the sources of conflict in previous phylogenomic studies. The Ulvophyceae is recovered as a paraphyletic group, with the Bryopsidales being a sister group to the Chlorophyceae, and the remaining taxa forming a clade (Ulvophyceae sensu stricto). Molecular clock analyses with different calibration strategies emphasize the large impact of fossil calibrations, and indicate a Meso-Neoproterozoic origin of the Ulvophyceae (sensu stricto), earlier than previous estimates. The results imply that ulvophyceans may have had a profound influence on oceanic redox structures and global biogeochemical cycles at the Mesoproterozoic-Neoproterozoic transition.

Fig. 1. Current knowledge of the phylogenetic relationships among the main lineages of the core Chlorophyta based on nuclear phylogenomic studies^,,.

Uncertain phylogenetic relationships are indicated by polytomies or dashed lines. The three different interpretations of the Proterocladus antiquus fossil, corresponding to the three strategies used in our dating analyses, are indicated with arrows: (1) Proterocladus as a total-group cladophoralean, (2) Proterocladus as a total-group ulvophycean, and (3) uncertain phylogenetic position (within or outside the green algae).

Fig. 2. Phylogenetic relationships of Ulvophyceae inferred from 884 nuclear genes.

A Species tree based on the multispecies coalescent model. Support for each node is provided by local posterior probability and multi-locus bootstrapping (PP/MLBS). Nodes without a value indicate full support. The pie charts at two focal nodes of Ulvophyceae present the proportion of gene tree concordance and conflict. Pie chart color coding: blue, fraction of gene trees that are concordant with the species tree; green, fraction of gene trees supporting the second most common conflicting topology; red, fraction of gene trees supporting all other alternative conflicting partitions; gray, fraction of gene trees with <50% bootstrap support at that node. The newly sampled species are marked with a symbol (*). Note that Desmochloris has been placed in the Chlorocystidales, and Pseudoneochloris has been recently placed in a new order, Sykidiales. B Topological comparison among coalescent- and concatenation-based analyses. Support for the conflicting branches is provided by PP/MLBS (in coalescent-based analysis) and SH-aLRT/ultrafast bootstrap (in concatenation-based analyses). The asterisk indicates support in the three analyses on the left. The source data of the pie charts in (A) are provided in the Source Data file.

Fig. 3. Gene tree discordance and coalescent simulations.

A The frequency of three topologies (q1–q3) around two short internal branches of ASTRAL species tree in the 69-taxon datasets. Each short internal branch with four neighboring branches leads to three possible topologies. B Phylogenetic relationships of 7-taxon(I) and 7-taxon(II) datasets based on the multispecies coalescent model. Red branches are the short branches. C Comparison of simulated frequencies of gene tree topologies with the corresponding observed frequencies. Bryo Bryopsidales, Chlo Chlorophyceae, Ulvo Ulvophyceae s.s.

Fig. 4. Comparison of divergence time estimates from three fossil assignment strategies.

The differences between the three calibration strategies refer to the placement of Proterocladus antiquus (strategy 1: P. antiquus to stem-group Cladophorales; strategy 2: P. antiquus to stem-group Ulvophyceae s.s.; strategy 3: exclusion of P. antiquus). Node ages are plotted at the posterior means, with horizontal bars representing 95% credibility intervals.