From ancient cold-blooded fishes to mammals, all vertebrates are protected by adaptive immunity, and retain immunological memory. Although immunologists can demonstrate these phenomena in all fish, the responding cells remain elusive for lack of defining markers and tools to study them. Fundamentally, we posited that it is longevity that defines a memory cell like how antibody production defines a plasma cell. We infected the common carp with Sphaerospora molnari, a cnidarian parasite which causes seasonal outbreaks to which no vaccine is available. B cells proliferated and expressed gene signatures of differentiation. Despite a half-year gap between EdU labeling and sampling, B cells retained the thymidine analogue, suggesting that these are at least six-month-old resting memory cells stemming from proliferating precursors. Additionally, we identified a lymphoid organ-resident population expressing exceptional levels of IgM as plasma cells. Thus, teleost fish produce the lymphocytes key to vaccination success and long-term disease protection, and immunological memory is universal and universally demonstrable.

Driven by co‐evolution with pathogens, host immunity continuously adapts to optimize defence against pathogens within a given environment. Recent advances in genetics, genomics and transcriptomics have enabled a more detailed investigation into how immunogenetic variation shapes the diversity of immune responses seen across domestic and wild animal species. However, a deeper understanding of the diverse molecular mechanisms that shape immunity within and among species is still needed to gain insight into—and generate evolutionary hypotheses on—the ultimate drivers of immunological differences. Here, we discuss current advances in our understanding of molecular evolution underpinning jawed vertebrate immunity. First, we introduce the immunome concept, a framework for characterizing genes involved in immune defence from a comparative perspective, then we outline how immune genes of interest can be identified. Second, we focus on how different selection modes are observed acting across groups of immune genes and propose hypotheses to explain these differences. We then provide an overview of the approaches used so far to study the evolutionary heterogeneity of immune genes on macro and microevolutionary scales. Finally, we discuss some of the current evidence as to how specific pathogens affect the evolution of different groups of immune genes. This review results from the collective discussion on the current key challenges in evolutionary immunology conducted at the ESEB 2021 Online Satellite Symposium: Molecular evolution of the vertebrate immune system, from the lab to natural populations.

Background Several hypotheses have been proposed to explain parasite infection in parental species and their hybrids. Hybrid heterosis is generally applied to explain the advantage for F1 generations of hybrids exhibiting a lower level of parasite infection when compared to parental species. Post-F1 generations often suffer from genetic incompatibilities potentially reflected in the higher level of parasite infection when compared to parental species. However, the presence of specific parasites in an associated host is also limited by close coevolutionary genetic host-parasite associations. This study focused on monogenean parasites closely associated with two leuciscid fish species—common bream and roach—with the aim of comparing the level of monogenean infection between parental species and hybrids representing two F1 generations with different mtDNA and two backcross generations with different cyto-nuclear compositions. Results Monogenean infection in F1 generations of hybrids was lower when compared to parental species, in line with the hybrid heterosis hypothesis. Monogenean infection in backcross generations exhibited similarities with the parental species whose genes contributed more to the backcross genotype. The distribution of monogeneans associated with one or the other parental species showed the same asymmetry with a higher proportion of roach-associated monogeneans in both F1 generations and backcross generation with roach in the paternal position. A higher proportion of common bream-associated monogeneans was found in backcross generation with common bream in the paternal position. Conclusions Our study indicated that cyto-nuclear incompatibilities in hybrids do not induce higher monogenean infection in backcross generations when compared to parental species. However, as backcross hybrids with a higher proportion of the genes of one parental taxon also exhibited high level of this parental taxon-associated parasites, host-parasite coevolutionary interactions seem to play an obvious role in determining the level of infection of host-specific monogeneans in hybrids.