Kin Interactions in a Colonial Hydrozoan (Hydractinia symbiolongicarpus): Population Structure on a Mobile Landscape

Abstract

Many sessile colonial organisms intensively compete with conspecifics for growing space. This competition can result in either cooperative fusion or aggressive rejection between colonies, and some species have evolved highly polymorphic genetic systems that mediate the outcome of these interactions. Here we demonstrate the potential for interactions among close kin as the basis for the evolutionary maintenance of a genetically polymorphic allorecognition system in the colonial hydroid Hydractinia symbiolongicarpus, which lives on gastropod shells occupied by hermit crabs. Fusion between hydroids in the laboratory is restricted mainly to encounters between full siblings, whereas other encounters result in aggressive rejection. Natural selection acting on the costs or benefits of fusion between colonies could be responsible for the present maintenance of such a highly specific behavioral response, but only if encounters between fusible colonies still occur in contemporary populations. The large size of these hydroid populations and the mobility of the crabs should limit the potential for interactions among closely related hydroids on the same shell. However, RAPD polymorphisms among a large sample of hydroids from a population off the coast of Massachusetts indicate that genetically similar colonies are often found together on the same shell. Some genetic distances between colonies on the same shell were low relative to genetic distances between colonies on different shells or genetic distances between known full siblings from laboratory matings. We conservatively estimate that 2-18% of co-occurring colonies may be full sibling pairs. These observations suggest that encounters between genetically similar hydroids are common, despite the mobile nature of their habitat, and these encounters may provide frequent opportunities for natural selection to influence the evolution of cooperative and agonistic behaviors and their polymorphic genetic basis.

Lessons in modularity: the evolutionary ecology of colonial invertebrates

“…Such expectation is reasonable, however, only if kin commonly grow into contact. Philopatric settlement of larval kin is documented for the cnidarian Hydractinia symbiolongicarpus (Hart and Grosberg, 1999), the bryozoan Bugula neritina (Keough, 1984) and the ascidian Botryllus schlosseri (Grosberg and Quinn, 1986). As predicted, histocompatibility measured by fusion frequency is positively correlated with kinship in the above species.…”

Gastropod shell size and morphology influence conspecific interactions in an encrusting hydroid

“…involve small, juvenile colonies (Yund et al 1987, Buss & Yund 1988, Buss & Grosberg 1990, Yund 1991, Hart & Grosberg 1999, Van Winkle & Blackstone 2002. The present study suggests that this conclusion is likely attributable to the size and species of gastropod shells available for Hydractinia spp.…”

“…Indeed, several studies have documented the frequent incidence of multiple colonization of a single shell and/or supply indirect evidence of interference competition between Hydractinia spp. conspecifics in natural populations (Yund et al 1987, Buss & Yund 1988, Yund & Parker 1989, Yund 1991, Hart & Grosberg 1999. In some cases, conspecific encounters may exceed even heterospecific encounters in frequency (Buss & Yund 1988).…”

Kinship and the evolution of social behaviours in the sea

“…In the sea, especially if most propagules have sufficient dispersal potential such that kin associations are likely to be rare, then it is less clear how selection would favour discrimination. However, in the above-mentioned cases, limited dispersal of sexual and asexual propagules [18], characteristic of many of clonal and even some aclonal marine organisms, coupled with the capacity for indeterminate growth and reproduction [19], intensify the likelihood of interactions between close relatives [15] (figure 1).…”