On Being a Monkey's Uncle: Germline Chimerism in the Callitrichinae and the Evolution of Sibling Rivalry

AbstractA typical monkey of the subfamily Callitrichinae has two or more cell lineages occupying its tissues: one from "itself," and one from its co-twin(s). Chimerism originates in utero when the twin placentae fuse, vascular anastomoses form between them, and cells are exchanged between conceptuses through their shared circulation. Previously it was thought that chimerism was limited to tissues of the hematopoietic cell lineage and that the germline was clonal, but subsequent empirical work has shown that chimerism may extend to many tissues, including the germline. To explore how natural selection on chimeric organisms should shape their social behavior, I construct an inclusive fitness model of sibling interactions that permits differing degrees of chimerism in the soma and germline. The model predicts that somatic chimerism should diminish sibling rivalry but that germline chimerism should typically intensify it. A further implication of the model is the possibility for intraorganismal conflict over developing phenotypes; as tissues may differ in their extent of chimerism-for example, placenta versus brain-their respective inclusive fitness may be maximized by different phenotypes. Communication between tissues in chimeric organisms might therefore be noisy, rapidly evolving, and fraught, as is common in systems with internal evolutionary conflicts of interest.