Abstract
BackgroundBotryllid ascidians are a group of marine invertebrate chordates that are colonial and grow by repeated rounds of asexual reproduction to form a colony of individual bodies, called zooids, linked by a common vascular network. Two distinct processes are responsible for zooid regeneration. In the first, called blastogenesis, new zooids arise from a region of multipotent epithelium from a pre-existing zooid. In the second, called whole body regeneration (WBR), mobile cells in the vasculature coalesce and are the source of the new zooid. In some botryllid species, blastogenesis and WBR occur concurrently, while in others, blastogenesis is used exclusively for growth, while WBR only occurs following injury or exiting periods of dormancy. In species such as Botrylloides diegensis, injury induced WBR is triggered by the surgical isolation of a small piece of vasculature. However, Botryllus schlosseri has unique requirements that must be met for successful injury induced WBR. Our goal was to understand why there would be different requirements between these two species.ResultsWhile WBR in B. diegensis was robust, we found that in B. schlosseri, new zooid growth following injury is unlikely due to circulatory cells, but instead a result of ectopic development of tissues leftover from the blastogenic process. These tissues could be whole, damaged, or partially resorbed developing zooids, and we defined the minimal amount of vascular biomass to support ectopic regeneration. We did find a common theme between the two species: a competitive process exists which results in only a single zooid reaching maturity following injury. We utilized this phenomenon and found that competition is reversible and mediated by circulating factors and/or cells.ConclusionsWe propose that WBR does not occur in B. schlosseri and that the unique requirements defined in other studies only serve to increase the chances of ectopic development. This is likely a response to injury as we have discovered a vascular-based reversible competitive mechanism which ensures that only a single zooid completes development. This competition has been described in other species, but the unique response of B. schlosseri to injury provides a new model to study resource allocation and competition within an individual.
Highlights
Botryllid ascidians are a group of marine invertebrate chordates that are colonial and grow by repeated rounds of asexual reproduction to form a colony of individual bodies, called zooids, linked by a common vascular network
We found that the zooid which develops after surgical isolation of blood vessels in B. schlosseri is not due to circulatory cells initiating whole body regeneration (WBR), but instead relies upon ectopic development of remnants of the blastogenic process
Disparities in injury response between phylogenetically related species Previous studies on whole body regeneration (WBR) in Botryllus schlosseri concluded that there were three requirements for zooid development from isolated vasculature: (1) experimental colonies must be large, having nine or more zooids [34]; (2) the marginal vessel, must be left intact following ablation of the zooids and buds for colony-wide circulation (Additional file 4: Video S2) [14]; and, (3) surgery required ablation of the zooids and buds when the zooids are resorbing during the takeover process [33, 34]
Summary
Botryllid ascidians are a group of marine invertebrate chordates that are colonial and grow by repeated rounds of asexual reproduction to form a colony of individual bodies, called zooids, linked by a common vascular network. Blastogenesis and WBR occur concurrently, while in others, blastogenesis is used exclusively for growth, while WBR only occurs following injury or exiting periods of dormancy In species such as Botrylloides diegensis, injury induced WBR is triggered by the surgical isolation of a small piece of vasculature. Many species are colonial [9] and propagate asexually This process, called budding, generates multiple independent individuals (called zooids) with a similar body plan to that of the oozooid [10,11,12,13,14]. Among the colonial species there are multiple asexual budding pathways that have arisen independently, and the diversity and phylogeny of these processes have been extensively reviewed [16,17,18]
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