Thaliaceans, The Neglected Pelagic Relatives of Ascidians: A Developmental and Evolutionary Enigma

Abstract

Most developmental biologists equate tunicates to the sessile ascidians, including Ciona intestinalis, and the pelagic appendicularians, in particular Oikopleura dioica. However, there exists a third group of tunicates with a pelagic lifestyle, the thaliaceans, which include salps, pyrosomes, and doliolids. Although thaliaceans have raised the curiosity offamous zoologists since the 18th century, the difficulty of observing and experimentally manipulating them has led to many controversies and speculations about their life cycles and developmental strategies, the phylogenetic relationship within the group and with other tunicates, and the drivers of speciation in these widely distributed animals living in a seemingly uniform environment. Here, we take a historical perspective to summarize 250 years of work on this intriguing group of animals, and explore how modern genomics and imaging approaches are starting to solve fascinating evolutionary and developmental riddles. Recent molecular analyses support previous morphological evidence that ascidians are not monophyletic and that thaliaceans evolved from a sessile ascidian-like ancestor. In parallel, preliminary live-imaging and gene-expression data offer exciting entry points to understand how the adoption of a pelagic lifestyle led to drastic modifications in the morphology, embryology, and life cycle of these tunicates, compared to their sessile ancestor.

A phylogenomic framework and timescale for comparative studies of tunicates

“…Even though the position of Thaliacea was not always statistically supported, it consistently appeared as the sister-group of phlebobranchs + aplousobranchs in previous studies [20,[24][25][26]28], except for a recent genome-scale study in which the positioning of Salpa thompsoni most likely suffered artefactual LBA attraction towards the fast-evolving appendicularians [66]. The robust phylogenetic position of thaliaceans found here indicates that they likely evolved from a sessile ancestor and their study can provide valuable information on the morphological transformations associated with the transition to the pelagic lifestyle [29].…”

“…Coloniality is another remarkable feature of the thaliaceans, which shows some similarities with the coloniality in ascidians, even tough this trait probably evolved independently in the two groups [29]. It is noteworthy that doliolids have polymorphic colonies [30], a trait that is absent in colonial ascidians.…”

“…The phylogenetic position of thaliaceans is key for understanding the evolution of developmental modes within tunicates [29]. Compared to their closest relatives that are mostly solitary and sessile, the three groups of thaliaceans (salps, doliolids and pyrosomes) are pelagic with complex life cycles including solitary and colonial phases.…”

“…Compared to their closest relatives that are mostly solitary and sessile, the three groups of thaliaceans (salps, doliolids and pyrosomes) are pelagic with complex life cycles including solitary and colonial phases. Their unique lifestyle also seems to be associated with spectacular differences in their embryology, such as the loss of a well-developed notochord in the larva of most thaliaceans, with the exception of only a few doliolid species [29]. Based on our current understanding of tunicate evolution, thaliaceans may have evolved from a sessile ascidian-like ancestor and therefore can serve as a model to understand how the transition from a benthic to a pelagic lifestyle has led to drastic modifications in the morphology, embryology, and life cycle of these tunicates [29].…”

Phylogenetic analysis of phenotypic characters of Tunicata supports basal Appendicularia and monophyletic Ascidiacea

“…The monophyly of Thaliacea is traditionally thought to be strongly supported (e.g. Govindarajan et al., ; see also review in Piette and Lemaire, ). A number of life‐history traits and phenotypic characters are usually interpreted as synapomorphies of thaliacean species.…”