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

Abstract

Volvocales forms a species‐rich clade with wide morphological variety and is regarded as an ideal model for tracing the evolutionary transitions in multicellularity. The phylogenetic relationships among the colonial volvocine algae and its relatives are important for investigating the origin of multicellularity in the clade Reinhardtinia. Therefore, a robust phylogenetic framework of the unicellular and colonial volvocine algae with broad taxon and gene sampling is essential for illuminating the evolution of multicellularity. Recent chloroplast phylogenomic studies have uncovered five major orders in the Chlorophyceae, but the family‐level relationships within Sphaeropleales and Volvocales remain elusive due to the uncertain positions of some incertae sedis taxa. In this study, we contributed six newly sequenced chloroplast genomes in the Volvocales and analyzed a dataset with 91 chlorophycean taxa and 58 protein‐coding genes. Conflicting phylogenetic signals were detected among chloroplast genes that resulted in discordant tree topologies among different analyses. We compared the phylogenetic trees inferred from original nucleotide, RY‐coding, codon‐degenerate, and amino acid datasets, and improved the robustness of phylogenetic inference in the Chlorophyceae by reducing base compositional bias. Our analyses indicate that the unicellular Chlamydomonas and Vitreochlamys are close to or nested within the colonial taxa, and all the incertae sedis taxa are nested within the monophyletic Sphaeropleales s.l. We propose that the colonial taxa in the Reinhardtinia are paraphyletic and multicellularity evolved once in the volvocine green algae and might be lost in Chlamydomonas and Vitreochlamys.

A Reinvestigation of Multiple Independent Evolution and Triassic–Jurassic Origins of Multicellular Volvocine Algae

“…Recent phylogenetic studies have indicated that the cellular differentiation and sexual reproduction patterns appear to multiple independent origins within the volvocine algae ( Grochau-Wright et al 2017 ; Hanschen et al 2018 ; Lindsey et al 2021 ). Notably, Li et al (2023) performed character estimation and supported the “secondary loss of multicellularity” scenario from the multicellular Tetrabaenaceae based on chloroplast phylogenomics. Li et al (2023) speculated that the Tetrabaena forms simple four-cell colonies and may not undergo incomplete cytokinesis like Goniaceae; thus, it implies possible reversions from multicellular Tetrabaenaceae ancestors to unicellular Vitreochlamys .…”

“…Notably, Li et al (2023) performed character estimation and supported the “secondary loss of multicellularity” scenario from the multicellular Tetrabaenaceae based on chloroplast phylogenomics. Li et al (2023) speculated that the Tetrabaena forms simple four-cell colonies and may not undergo incomplete cytokinesis like Goniaceae; thus, it implies possible reversions from multicellular Tetrabaenaceae ancestors to unicellular Vitreochlamys . These results suggested that the evolutionary history of the volvocine algae is complex than expected.…”

“…Instead, the chloroplast phylogenomic analyses uncovered the close relationship between the Sphaeropleales and some incertae sedis taxa ( Lemieux et al 2015 ; Fučíková et al 2019 ). In addition, nuclear ribosomal and chloroplast multigene data produced inconsistent results among the main clades of the Volvocales ( Nakada et al 2008 ; Lemieux et al 2015 ; Fučíková et al 2019 ; Li et al 2023 ); especially, the monophyly of colonial TGV clade has been controversial. Early phylogenetic studies based on few chloroplast genes have uncovered the monophyly of the colonial algae ( Nozaki et al 2000 ; Herron and Michod 2008 ; Herron et al 2009 ; Nakada et al 2010 ; Nozaki et al 2014 ), which was also supported by Hu et al (2019 , 2020) .…”

“…Early phylogenetic studies based on few chloroplast genes have uncovered the monophyly of the colonial algae ( Nozaki et al 2000 ; Herron and Michod 2008 ; Herron et al 2009 ; Nakada et al 2010 ; Nozaki et al 2014 ), which was also supported by Hu et al (2019 , 2020) . However, phylogenetic analyses based on chloroplast genomes or multiple nuclear genes rejected the monophyly of the colonial TGV clade and indicated that several Chlamydomonas and Vitreochlamys species were close to the colonial volvocine algae ( Pröschold et al 2018 ; Nakada et al 2019 ; Li et al 2023 ). Recently, Lindsey et al (2021) recovered the nonmonophyletic colonial volvocine algae and showed that multicellularity independently evolved at least twice in the volvocine algae.…”

Phylogenomics, divergence time estimation, and adaptive evolution in the Polygonoideae (Polygonaceae)

“…Complete plastomes contain variants that can provide sufficient phylogenetic information to distinguish closely related species (Wen et al, 2021; Cao et al, 2022; Li et al, 2022), including Polygonaceae species with complex evolutionary histories, such as Atraphaxis and Fagopyrum (Xu & Zhang, 2015; Fan et al, 2021; Wen et al, 2021). In addition to their applicability for phylogenetic studies, complete plastomes can provide insights into other evolutionary processes, such as chloroplast inheritance and adaptive evolution (Liu et al, 2021; Wen et al, 2021; Li et al, 2022). Furthermore, using plastome data to reconstruct phylogenetic relationships and identify ancestral states in a temporal context can provide a better understanding of the evolutionary history (Zhang et al, 2014; Yao et al, 2019).…”