Histocompatibility as Adaptive Response to Discriminatory Within-Organism Conflict: A Historical Model

Abstract

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Online enhancement: appendix.abstract: Multicellular tissue compatibility, or histocompatibility, restricts fusion to close kin. Histocompatibility depends on hypervariable cue genes, which often have more than 100 alleles in a population. To explain the evolution of histocompatibility, I here take a historical approach. I focus on the specific example of marine invertebrate histocompatibility. I use simple game-theoretical models to show that histocompatibility can evolve through five steps. These steps include the evolution of indiscriminate fusion, the evolution of discriminatory within-organism conflict, the evolution of minor histocompatibility, the evolution of major histocompatibility, and the evolution of major histocompatibility cue polymorphism. Allowing for gradual evolution reveals discriminatory within-organism conflict as a selective pressure for histocompatibility and associated cue polymorphism. Existing data from marine invertebrates and other organisms are consistent with this hypothesis.

Rapid and widespread de novo evolution of kin discrimination

“…Crozier proposed that some "extrinsic" factor other than direct selection on kin-discriminatory interactions is necessary for the maintenance of diverse social allotypes because positive frequency-dependent selection on cooperative traits is expected to favor the most common social allotype (11,16,37,38). Our results suggest that, at least in some biological systems, stochastic variation in adaptive trajectories may generate novel allotypes more rapidly than the most common allotype in a local population can increase toward fixation.…”

Microscale kin discrimination in a famous soil bacterium

“…Second, an assumption of somatic compatibility in B. subtilis yields explanatory coherence. Stefanic et al's (6) finding of variability in morphology of boundary lines in fusion events between close relatives is reminiscent of what is seen in marine invertebrates, true slime molds, and fungi, where somatic compatibility reactions often become variable and delayed with fusion between close kin (12,16,17). A possible genetic explanation for this is that nonclonemate kin differ at only one or two of multiple somatic compatibility cue genes, with each gene having a different effect.…”

“…Buss (10,11) argued that multicellular organisms that fuse exist in part because they possess somatic compatibility systems that restrict fusion to close kin, and prevent the spread of somatic cell parasites that threaten somatic differentiation. Although the Hamilton and Buss views on kin discrimination are often viewed as synonymous, a recent model shows that somatic compatibility can evolve in response to discriminating nepotism (12). This model suggests discriminating nepotism can involve behaviors that preferentially rob nonkin of somatic resources, and that the evolution of somatic compatibility in response to these discriminatory behaviors incidentally prevents the spread of cancer-like somatic parasites (12).…”

“…Although the Hamilton and Buss views on kin discrimination are often viewed as synonymous, a recent model shows that somatic compatibility can evolve in response to discriminating nepotism (12). This model suggests discriminating nepotism can involve behaviors that preferentially rob nonkin of somatic resources, and that the evolution of somatic compatibility in response to these discriminatory behaviors incidentally prevents the spread of cancer-like somatic parasites (12).…”

“…Viewed from the biofilm as a whole, these valuable cellular behaviors constitute a somatic resource that could be robbed by nonkin when fusion occurs. The resulting conflicts would be predicted to select for somatic compatibility (12). Second, an assumption of somatic compatibility in B. subtilis yields explanatory coherence.…”