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

Abstract

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 evolutionary history of this group have often relied on datasets of one to a few genes for phylogenetic inference and ancestral character state reconstruction. These 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. We performed RNA-Seq on 55 strains representing 47 volvocine algal species, and obtained similar data from curated databases on 13 additional strains. We generated a dataset consisting of transcripts for 40 single-copy, protein-coding, nuclear genes, then 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 independently arose at least four and possibly as many as six times within the group. Altogether, these results show how multicellularity and cellular differentiation are evolutionarily labile in the volvocine algae, affirming their importance for the study of major transitions in the history of life.

Chloroplast phylogenomics of unicellular and colonial Volvocales provides perspectives on the evolution of morphological characters

“…3, S4), and the close relationship between C. reinhardtii and the colonial Goniaceae + Volvocaceae clade (Figs. S6-S8) have been reported in previous studies using multigene (Nozaki et al, 2003;Pröschold et al, 2018;Nakada et al, 2019) or transcriptomic data (Lindsey et al, 2021). Morphologically, the conversion of the cell wall into ECM was an essential step in colonial algae (e.g., Tetrabaenaceae), and was absent in the unicellular lineages (Kirk, 2005;Herron & Michod, 2008;Hanschen et al, 2017).…”

“…It is worth noting that, different from the chloroplast phylogenomic studies, Nakada et al (2008) regarded Spermatozopsis, Treubarinia, and Golenkinia as volvocalean members. Recent phylogenetic studies based on 18S and five chloroplast genes from Nakada et al (2019) and 40 nuclear genes from Lindsey et al (2021) focused exclusively on the Chlamydomonas, Vitreochlamys and Tetrabaenaceae-Goniaceae-Volvocaceae (TGV) clade in the Reinhardtinia, and discussed the origin of coloniality with increasing unicellular and colonial species. Therefore, volvocine algae are ideal model organisms for tracing the processes that have shaped the initial advent of multicellularity (Kirk, 2005;Herron & Michod, 2008;Hallmann, 2011;Herron & Nedelcu, 2015;Herron et al, 2009Herron et al, , 2019.…”

“…Previous phylogenetic studies have uncovered the monophyly of the colonial TGV clade in the Reinhardtinia based on chloroplast genomes (Fučíková et al, 2019;Hu et al, 2019aHu et al, , 2019b and 105 single-copy nuclear genes (Hu et al, 2020). This might be due to the lack of key unicellular Chlamydomonas and Vitreochlamys taxa that were found nested within the colonial clade in Nakada et al (2019) and Lindsey et al (2021) as mentioned above, and studies using plastid rbcL gene or the nuclear ITS region (Nakazawa et al, 2001;Pröschold et al, 2018). Therefore, the phylogenetic relationships and the evolutionary history of the volvocine algae have lacked concordance in previous studies, and it is challenging to balance taxon and gene sampling.…”

“…They were based on one or a few genes with broad volvocine algae taxa (Nozaki et al, 2003;Herron & Michod, 2008;Pröschold et al, 2018;Nakada et al, 2019) or on genome-scale chloroplast data with limited taxon sampling (Fučíková et al, 2019;Hu et al, 2019aHu et al, , 2019b. Therefore, unicellular Chlamydomonas and Vitreochlamys are crucial for understanding the evolution of multicellularity in the TGV clade (Kirk, 2005;Umen, 2014Umen, , 2020Nakada et al, 2019;Lindsey et al, 2021), and it is necessary to carry out dedicated studies including more Chlamydomonas and Vitreochlamys samples and more genes.…”

Cryopreservation of two species of the multicellular volvocine green algal genus Astrephomene

“…1), show similar or convergent evolution of multicellular spheroidal bodies with germ-soma differentiation (Additional le 1: Fig. S1) [3][4][5]. Whole-genome sequencing of A. gubernaculifera provided insight into the molecular-genetic basis of such convergent evolution [6].…”