Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae

Abstract

Background The volvocine algae, which include the single-celled species Chlamydomonas reinhardtii and the colonial species Volvox carteri, serve as a model in which to study the evolution of multicellularity and cellular differentiation. Studies reconstructing the history of this group have by and large relied on datasets of one to a few genes for phylogenetic inference and ancestral character state reconstruction. As a result, volvocine phylogenies lack concordance depending on the number and/or type of genes (i.e., chloroplast vs nuclear) chosen for phylogenetic inference. While multiple studies suggest that multicellularity evolved only once in the volvocine algae, that each of its three colonial families is monophyletic, and that there have been at least three independent origins of cellular differentiation in the group, other studies call into question one or more of these conclusions. An accurate assessment of the evolutionary history of the volvocine algae requires inference of a more robust phylogeny. Results We performed RNA sequencing (RNA-seq) on 55 strains representing 47 volvocine algal species and obtained similar data from curated databases on 13 additional strains. We then compiled a dataset consisting of transcripts for 40 single-copy, protein-coding, nuclear genes and subjected the predicted amino acid sequences of these genes to maximum likelihood, Bayesian inference, and coalescent-based analyses. These analyses show that multicellularity independently evolved at least twice in the volvocine algae and that the colonial family Goniaceae is not monophyletic. Our data further indicate that cellular differentiation arose independently at least four, and possibly as many as six times, within the volvocine algae. Conclusions Altogether, our results demonstrate that multicellularity and cellular differentiation are evolutionarily labile in the volvocine algae, affirming the importance of this group as a model system for the study of major transitions in the history of life.

Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation

“…gubernaculifera and genome data of other volvocine algae (see Supplementary Methods ) positioned Astrephomene as a sister group of Volvocaceae (Supplementary Fig. 4 ), which is consistent with the recent phylotranscriptomic analysis of volvocine species 38 .…”

“…The phylogenetic relationships are based on the present phylogenomic analysis (Supplementary Fig. 4 ) and a previous report 38 . The genomes of all genera except for Astrephomene have been sequenced in previous studies 7 – 11 .…”

The Curious Case of Multicellularity in the Volvocine Algae

“…The volvocines are a well-established model system for the study of multicellularity ( Nedelcu and Michod, 2003 ; Kirk, 2005 ; Miller and Technau, 2010 ; Niklas, 2014 ; Grochau-Wright et al, 2017 ) that encompasses ∼50 extant multicellular species and their closest unicellular relative, Chlamydomonas reinhardtii ( Kirk, 1997 ; Coleman, 1999 ; Umen and Olson, 2012 ) ( Figure 1A ). Multicellular volvocines are arranged into families Tetrabaenaceae ( Basichlamys, Tetrabaena ), Goniaceae ( Gonium, Astrephomene ) and Volvocaceae ( Pandorina, Eudorina, Yamagishiella, Volvox ) ( Hanschen et al, 2018a ; Lindsey et al, 2021 ), and display morphologies ranging from bowl-shaped undifferentiated colonies to differentiated spheroids ( Kirk, 1997 ; Coleman, 2012 ; Yamashita et al, 2016 ) ( Figure 1A ). Despite their phenotypic differences, this diverse group of algae evolved from their Chlamydomonas- like unicellular ancestor relatively recently during the Triassic period (around 250 MYA) ( Herron et al, 2009 ).…”

“… The evolution of volvocine developmental complexity is marked by gains and losses of traits. Adapted from ( Ruiz-Trillo and Nedelcu, 2015 ; Lindsey et al, 2021 ). (A) Phylogeny of the volvocine algae.…”

“…Unlike the initial shift to undifferentiated multicellularity that was likely boosted by co-option of RB , it would seem like subsequent genetic changes related to ECM maintenance, inversion, and cell differentiation have roles in stabilizing colonial life and controlling subsequent developmental processes rather than impacting multicellularity itself ( Figure 1B ). Indeed, Kirk’s streamlined framework has undergone revisions in light of the discovery of a dynamic history of gains and losses of morphological and developmental traits ( Nanjundiah et al, 2018 ; Lindsey et al, 2021 ) ( Figure 1A ). Hence, the volvocine phylogenetic tree is under constant revision ( Nozaki et al, 2003 ; Hanschen et al, 2018b ; Lindsey et al, 2021 ).…”