Ontogenetic changes in fusibility in the colonial hydroid Hydractinia symbiolongicarpus

Invertebrate fusion and rejection responses are typically assumed to be mutually exclusive and temporally stable states. We here describe a segregant class appearing in an F, cross of the colonial hydroid, Hydractinia syrnbiolongicarpus, that displays an ontogenetic change in fusibility. Reproductively immature offspring fuse to parental strains and have been observed to remain continuously fused for up to 76 days. By contrast, reproductively mature offspring initially fused with parental strains, only to separate into distinct colonies after a period of 3-21 days postfusion. Experimental manipulations demonstrate that (1) ontogenetic changes in fusibility cannot be removed by resetting a colony to a reproductively immature state, and (2) secondary contact does not result in an accelerated response. Although invertebrate allorecognition re- sponses have been known since the turn of the century (e.g., see Bancroft, '031, study of the popu- lation dynamic consequences of invertebrate fu- sion and rejection responses is a relatively recent undertaking (Buss, '82, '87; Grosberg, '88; Gros- berg and Quinn, '88). Fusion results in a number of direct advantages to the individuals that fuse. Colonies that fuse increase their size by doing so, and increased size is favored if the risk of mortal- ity is high either at small colony size, or if fecun- dity increases with colony size, or both. Many, if not most, colonial marine invertebrates are char- acterized by just such a size-specific schedule of mortality and fecundity (Jackson, '85). In addi- tion, size increase, hence fusion, may be expected to hasten the age of first reproduction, and this trait is known to be an especially important de- mographic character for organisms living in sea- sonal environments (Cole, '54). Given the apparent benefits to fusion, it may appear odd that any colony should fail to fuse with a conspecific. Although concrete benefits accrue to fusion, there are attendant costs. All colonial invertebrate taxa possess a mitotically active, multipotent stem cell lineage that is com- petent to produce gametes throughout ontogeny (Nieuwkoop and Sutasurya, '81; Buss, '83). If fu- sion results in exchange of stem cells from one colony to another, the potential exists for one component of the chimera to contribute dispropor- tionately to the gamete production (Buss, '82, '87). Such "somatic cell parasitism" has been docu- 0 1991 WILEY-LISS, INC. mented in the cellular slime mold Dictyostehm (Buss, '82), the hydroid Hydractinia (Hauen- schild, '54; Muller, '64; Buss and Shenk, '901, and the ascidian, Botryllus (Sabbadin and Zaniolo, '79; Sabbadin and Astorri, '89; R. Grosberg, per,- sonal communication; I. Weissman, personal com- munication). Given that the benefits of fusion would appear to accrue at small colony size and the costs of fu- sion appear to accrue at reproductive maturity, one might reasonably expect to encounter organ- isms that display an ontogenetic change in fusi- bility. Two such cases have been suggested. Al- logeneic primary polyps of the scleractinian coral Pocillopora damicornis derived from different matings have been shown to fuse, whereas the maternal parents from which these primary polyps were derived display a typical rejection (Hikada, '85). A second potential case of an on- togenetic change in fusibility is suggested by an anecdotal observation reported by Hauenschild ('54) in his work with athecate hydroid Hydrac- tinia echinata. He noted that attempts to produce intersexual chimeras by fusing two reproduc- tively mature colonies failed despite the fact that he had observed fusion between the same two clones as juveniles. We have attempted to confirm and extend Hauenschild's observation using a Western At-