Convergent Acquisition of Nonembryonic Development in Styelid Ascidians

Abstract

Asexual propagation and whole body regeneration are forms of nonembryonic development (NED) widespread across animal phyla and central in life history and evolutionary diversification of metazoans. Whereas it is challenging to reconstruct the gains or losses of NED at large phylogenetic scale, comparative studies could benefit from being conducted at more restricted taxonomic scale, in groups for which phylogenetic relationships are well established. The ascidian family of Styelidae encompasses strictly sexually reproducing solitary forms as well as colonial species that combine sexual reproduction with different forms of NED. To date, the phylogenetic relationships between colonial and solitary styelids remain controversial and so is the pattern of NED evolution. In this study, we built an original pipeline to combine eight genomes with 18 de novo assembled transcriptomes and constructed data sets of unambiguously orthologous genes. Using a phylogenomic super-matrix of 4,908 genes from these 26 tunicates we provided a robust phylogeny of this family of chordates, which supports two convergent acquisitions of NED. This result prompted us to further describe the budding process in the species Polyandrocarpa zorritensis, leading to the discovery of a novel mechanism of asexual development. Whereas the pipeline and the data sets produced can be used for further phylogenetic reconstructions in tunicates, the phylogeny provided here sets an evolutionary framework for future experimental studies on the emergence and disappearance of complex characters such as asexual propagation and whole body regeneration.

Conservation of peripheral nervous system formation mechanisms in divergent ascidian embryos

“…While we have obtained these results on a limited number of CRMs and while we have not tested CRMs from M. appendiculata whose genome has not been sequenced, we believe that, taking expression patterns into account, M. appendiculata is the divergent species among all species that we have used ( Figure 10). Our hypothesis is in agreement with previous CRM swap experiments between Ciona and other Molgula species (26), with the facts that Molgula is a fast evolving genus within ascidians (41,62) and that Molgulids is a family where loss of chordate body plan has occurred several times independently (tail-less larvae) (63). Egg dechorionation was performed before fertilization for P. fumigata and A. mentula as previously described for P. mammillata (14), and after fertilization for M. appendiculata as described for C. intestinalis (69).…”

Integrin-alpha-6+ Candidate stem cells are responsible for whole body regeneration in the invertebrate chordate Botrylloides diegensis

“…Zooids have a complex anatomy: they are filter feeders with siphons and a branchial basket, gastrointestinal tract, central and peripheral nervous system, endocrine glands, a heart, and a circulatory system consisting of 8-12 blood cell types. In colonial ascidians that belong to the Botryllinae, such as B. diegensis, zooids reproduce asexually, and the adult body plan consists of a colony of clonally derived individuals 5,[10][11][12][13][14] embedded within a gelatinous structure called a tunic (Fig. 1a).…”

Modular co-option of cardiopharyngeal genes during non-embryonic myogenesis

“…However, without live tracking, the dynamic nature of muscle formation cannot be fully understood, and we cannot rule out that the Mrf+ cells originate from other domains. Because muscle cell fates from these precursors have not been reported in Ciona, nor could we detect any such muscle fates in other closely related styelid species 54 (Supp. Fig.…”