Retreat Growth in the Ascidian Botryllus Schlosseri: A Consequence of Nonself Recognition

Abstract

In the genus Botryllus fusion between genetically distinct individuals is controlled by a single genetic locus (or haplotype) with multiple codominantly expressed alleles. Colonies which do not share an allele at this locus reject each other. The outcomes of juxtaposing nonfusible colonies of the colonial ascidian Botryllus schlosseri from Monterey, California, were followed in terms of colony rejection and colony vectorial growth in two sets of experiments. In the first, 2–5 subclones were isolated from each of 14 large colonies and experimentally matched to 26 nonfusible pairs. In the second, 50 nonfusible pairs of oozooids were followed for up to one year. A rejection between two allogeneic colonies was documented 24h to 3 days after first tunic-tunic contact was observed, although ampullae actually did not penetrate into the tunic of the opposing colony and the outer layers of the tunics were demarcated even after rejection took place. Points of rejection (POR) were recorded either in the tunic margin of one colony or in both. In 18 pairs of oozooids, no POR was recorded months after tunic-tunic and ampulla-ampulla contacts were established. After the first POR was formed, others usually were added within 1–7 days; thereafter no more occurred. Simultaneously, some or most interacting ampullae of either one or both sides moved back. Others disintegrated or narrowed. During and after these events, many colonies changed direction of growth and started to grow away from areas of contact. This change in vectorial growth was recognized 1–2 weeks after rejection and was produced either by one or both partners in a pair. This phenomenon is termed “retreat growth.” Five characteristics of this phenomenon are experimentally illustrated: 1. Whenever retreat growth occurs, all subclones from the same colony repeatably retreat when paired with non-fusible colonies. Similarly, retreat growth occurs in a second set of experiments done with the same set of subclones. 2. The retreat growth phenomenon in non-fusible colonies is independent of whether the colonies reject or not. A retreat growth developed in 7 out of the 18 pairs in which no point of rejection was recorded. 3. Retreat growth of rejecting pairs proceeds only after establishment of PORs. 4. The retreat growth phenomenon usually occurs during the takeover phase of the old generation of zooids. The new generation of blastozooids facing the POR area fail to develop to a mature phase, and resorb, while distant zooids successfully complete their development. 5. Retreat growth significantly reduces the time required for disconnection between two interacting colonies, compared to pairs in which this phenomenon is absent. The occurrence of similar retreat growth phenomena in other colonial invertebrates from the Cnidaria and the Porifera are cited and compared. It is proposed that the retreat growth phenomenon in B. schlossen is genetically controlled and is the consequence of self/nonself recognition, independent of colonial rejection (colony specificity). The retreat growth phenomenon, coupled with the eventual disintegration of the tunic between interacting colonies, promotes separation of nonfusible colonies, with no recorded deleterious effect to the survivorship of either one of the interacting colonies.