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Phylogenetically conserved peritoneal fibrosis response to an immunologic adjuvant in ray-finned fishes

Abstract

Maintenance of body homeostasis and protection from infection are fundamental to survival. While recognition of self and non-self appeared early in the evolution of metazoans, immunity remains one of the fastest evolving traits to keep up with dynamic challenges from parasites. The immune system thus intertwines ancient innate immune pathways with recently evolved adaptive pattern-recognition units. Here, we focus on peritoneal fibrosis, an effective, yet costly, defense to eliminate infection by a specialist tapeworm parasite, Schistocephalus solidus (Cestoda), observed in only some populations of threespine stickleback (Gasterosteus aculeatus, Perciformes). We asked whether stickleback fibrosis is a derived species-specific trait or an ancestral immune response that was widely distributed across ray-finned fish (Actinopterygii). First, we reviewed literature published on fibrosis in fish in general and found that peritoneal fibrosis specifically is very rarely reported in ray-finned fish. Then, we experimentally tested for peritoneal fibrosis with parasite-specific and non-specific immune challenges in deliberately selected species across fish tree of life. Peritoneal injection with a common non-specific vaccination adjuvant (Alum) showed that most of the tested species were capable to develop fibrosis. On the other hand, the species were largely indifferent to the tapeworm antigen homogenate. One specific fish clade – Characidae - did not respond to any of the treatments. We therefore show that despite being rarely reported in the literature, peritoneal fibrosis is a common and deeply conserved fish response to a non-specific immune challenge. We outline directions for further research on mechanisms and evolution of peritoneal fibrosis in fish, and also discuss new perspective on peritoneal fibrotic pathology in human patients.

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