The Evolution of Allorecognition Specificity

Abstract

Sessile, clonal invertebrates frequently encounter conspecifics as they grow over hard substrata and compete for space. Allorecognition systems mediate the nature and outcomes of these encouters by controlling somatic compatibility (fusion versus nonfusion) and agonistic behavior (aggression versus nonaggression). In general, clonemates (and sometimes close relatives) can fuse somatically, whereas more distant relatives are incompatible. Many anthozoan and hydrozoan cnidarians behave passively when in contact with clonemates and close kin, but fight aggressibely when contacting more distant relatives. This high degree of allorecognition specificity, when considered togehter with the few available data on the formal genetics of allorecognition, suggests that levels of polymorphism at allorecognition loci (i.e., allotypic variation) exceed by perhaps an order of magnitude the levels typical of other polymorphic loci. In this paper, I evaluate the strengths and weaknesses of the selectionist and nonselectionist theories that have been proposed to account for the evolution and persistence of allotypic polymorphism. It remains difficult to accept or reject any of these hypotheses in the absence of detailed empirical information concerning levels and patterns of allelic variation at allorecognition loci. Nevertheless, mathematical considerations and the available data together suggest that frequency-dependent or spatially variable selection are the strongest candidates for the maintenance of allotypic variation. Although the pleiotropic effects of allorecognition loci (e.g., the regulation of gametic compatibility or pathogenic defense) could maintain allotypic variation, pleiotropy by itself does not account for the widespread evolution of aggressive behavior and somatic compatibility conditioned by allotypic similarity. It is theoretically possible that frequency-dependent selection acting at the level of the individual maintains allotypic polymorphism by restricting somatic fusion; it is less clear how individual selection maintains allotypic variation through the regulation of agonistic behavior.