Our understanding of the vertebrate immune system is dominated by a few model organisms such as mice. This use of a few model systems is reasonable if major features of the immune systems evolve slowly and are conserved across most vertebrates, but may be problematic if there is substantial macroevolutionary change in immune responses. Here, we present a test of the macroevolutionary stability, across 15 species of jawed fishes, of the transcriptomic response to a standardized immune challenge. Intraperitoneal injection of an immune adjuvant (alum) induces a fibrosis response in nearly all jawed fishes, which in some species contributes to anti-helminth resistance. Despite this conserved phenotypic response, the underlying transcriptomic response is highly inconsistent across species. Although many gene orthogroups exhibit differential expression between saline versus alum-injected fish in at least one species, few orthogroups exhibit consistent differential expression across species. This result suggests that although the phenotypic response to alum (fibrosis) is highly conserved, the underlying gene regulatory architecture is very flexible and cannot readily be extrapolated from any one species to fishes (or vertebrates) more broadly. The vertebrate immune response is remarkably changeable over macroevolutionary time, requiring a diversity of model organisms to describe effectively.

• Keywords
• evolutionary immunology, fibrosis, transcriptome,
• Publication type
• Journal Article MeSH
• Preprint MeSH

Antagonistic interactions between hosts and parasites may drive the evolution of novel host defenses, or new parasite strategies. Host immunity is therefore one of the fastest evolving traits. But where do the novel immune traits come from? Here, we test for phylogenetic conservation in a rapidly evolving immune trait-peritoneal fibrosis. Peritoneal fibrosis is a costly defense against a specialist tapeworm, Schistocephalus solidus (Cestoda), expressed in some freshwater populations of threespine stickleback fish (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) only to be employed by threespine stickleback against the specialist parasite. We combined literature review on peritoneal fibrosis with a comparative experiment using either parasite-specific, or nonspecific, immune challenge in deliberately selected species across fish tree of life. We show that ray-finned fish are broadly, but not universally, able to induce peritoneal fibrosis when challenged with a generic stimulus (Alum adjuvant). The experimental species were, however, largely indifferent to the tapeworm antigen homogenate. Peritoneal fibrosis, thus, appears to be a common and deeply conserved fish immune response that was co-opted by stickleback to adapt to a new selective challenge.

• Keywords
• Actinopterygii, comparative experiment, immunity, peritoneal fibrosis, stickleback, vaccination,
• MeSH
• Cestoda * MeSH
• Cestode Infections * MeSH
• Phylogeny MeSH
• Fish Diseases * MeSH
• Immunity, Innate MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH