Evolution and development of budding by stem cells: Ascidian coloniality as a case study

Abstract

The evolution of budding in metazoans is not well understood on a mechanistic level, but is an important developmental process. We examine the evolution of coloniality in ascidians, contrasting the life histories of solitary and colonial forms with a focus on the cellular and developmental basis of the evolution of budding. Tunicates are an excellent group to study colonial transitions, as all solitary larvae develop with determinant and invariant cleavage patterns, but colonial species show robust developmental flexibility during larval development. We propose that acquiring new stem cell lineages in the larvae may be a preadaptation necessary for the evolution of budding. Brooding in colonial ascidians allows increased egg size, which in turn allows greater flexibility in the specification of cells and cell numbers in late embryonic and pre-metamorphic larval stages. We review hypotheses for changes in stem cell lineages in colonial species, describe what the current data suggest about the evolution of budding, and discuss where we believe further studies will be most fruitful.

Reconsidering regeneration in metazoans: an evo-devo approach

“…Studying the adaptability of regeneration is certainly not a simple task, however, in organisms where regeneration is tightly linked to asexual propagation, coloniality and their life history strategies (Berrill, 1951;Bely and Wray, 2001;Kawamura et al, 2008;Tiozzo et al, 2008;Burton and Finnerty, 2009;Brown and Swalla, 2012). It is likely that regeneration traits are subject to selection, mainly because they may be directly linked to reproductive success.…”

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

“…The crucial contribution of his friend Eschscholtz, and the rather skeptical reception of his discovery by his colleagues are nicely described by Glaubrecht and Dohle (2012). Each species possesses a solitary form, which gives rise to a chain of aggregate forms by budding from what is generally called a stolon, although this structure is most likely not homologous to the homonymous organ of other ascidians such as Perophora (Brown and Swalla 2012). The aggregate form then reproduces sexually to give rise to the solitary form, closing the cycle:…”

“…This debate is not only semantic, but is of importance for the role of the separation of germ line and soma in salp evolution, since a partial separation could lead to the incorporation of somatic mutations in the germ line (see Buss 1987). The origin of germ cells in salps has not been demonstrated conclusively, but could now be traced by following the expression of molecular markers such as vasa (Brown and Swalla 2012;Box 2).…”

“…In contrast to ascidians, which display a wide range of budding strategies (Brown and Swalla 2012), differences between pyrosomes, salps, and doliolids remain subtle, and argue for the single emergence, or monophyly, of the group (see below). In pyrosomes, the stolon of the blastozooids is the prolongation of that of the cyathozooid and the ascidiozooids, but it is fragmented and not continuous as in salps and doliolids (Brien 1948).…”

“…Neoteny: the somatic development of an organism is slowed or delayed leading to paedomorphosis Oozooid: zooid obtained by embryogenesis from an egg Paedomorphosis: the retention by adults of traits previously seen only in juveniles Phorozooid: zooid of doliolids specialized in carrying and dissemination of the gonozooids Protogynic: hermaphrodites in which eggs mature before sperm Pyrosoma ambulacria: a subgroup of pyrosomes with wandering buds (has no systematic value), in contrast to Pyrosoma fixata, in which the buds remain fixed Rhabdomeric photoreceptors: photoreceptors with arrays of microvilli rather than cilia as in the ciliary photoreceptors Stolon: in its narrow sense, a vasculature that connects individuals of colonial ascidians that are generally separated in their own tunic (Brown and Swalla 2012); in thaliaceans, also used in a broader sense to designate the organ from which the blastozooids bud or strobilize Strobilization: budding in colonial aplousobranch ascidians that occur from constriction of pieces that detach at the posterior-abdominal end of individuals (Brown and Swalla 2012); in thaliaceans, also used to designate the constriction of buds from the stolon Thecogonta: salpa with embryos protected by an amnionlike fold (has no systematic value) Trophozooids: zooids of doliolids specialized in feeding of the colony…”