Immunoglobulins (Igs) in mucosal secretions contribute to immune homeostasis by limiting access of microbial and environmental antigens to the body proper, maintaining the integrity of the epithelial barrier and shaping the composition of the commensal microbiota. The emergence of IgM in cartilaginous fish represented the primordial mucosal Ig, which is expressed in all higher vertebrates. Expansion and diversification of the mucosal Ig repertoire led to the emergence of IgT in bony fishes, IgX in amphibians, and IgA in reptiles, birds, and mammals. Parallel evolution of cellular receptors for the constant (Fc) regions of Igs provided mechanisms for their transport and immune effector functions. The most ancient of these Fc receptors is the polymeric Ig receptor (pIgR), which first appeared in an ancestor of bony fishes. The pIgR transports polymeric IgM, IgT, IgX, and IgA across epithelial cells into external secretions. Diversification and refinement of the structure of mucosal Igs during tetrapod evolution were paralleled by structural changes in pIgR, culminating in the multifunctional secretory IgA complex in mammals. In this paper, evidence is presented that the mutualistic relationship between the commensal microbiota and the vertebrate host provided the driving force for coevolution of mucosal Igs and pIgR. 1. Introduction The mucosal surfaces of the body form the primary interface with the outside world, providing a conduit for intake of nutrients and air and a home for beneficial microbes that act as “extended self” [1]. Host cells that populate mucosal surfaces must carry out the challenging task of maintaining a mutualistic relationship with the resident microbiota, while protecting the body proper against potential pathogens, toxic environmental substances, and soluble dietary antigens that could act as systemic allergens. Adaptive immune systems, characterized by clonally expressed, somatically diversified antigen receptors in lymphocytes, first emerged in a common ancestor of modern vertebrates [2, 3] (Figure 1). Jawless fish of the superclass Agnatha (hagfishes and lampreys) generate variable-like receptors (VLRs) for antigen (Ag) by a mechanism involving gene conversion. The evolution of the RAG1/2 dependent mechanism of V(D)J somatic recombination in an ancestor of modern jawed vertebrates led to the first appearance of Ag-specific immunoglobulins (Igs) and T-cell antigen receptors [4, 5]. The basic structural unit of Igs comprises 2 identical light chains, encoded by IGL genes, and 2 identical heavy chains, encoded by IGH genes
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