A Comparison of the Innate and Adaptive Immune Systems in Cartilaginous Fish, Ray-Finned Fish, and Lobe-Finned Fish

Abstract

The immune system is composed of two subsystems-the innate immune system and the adaptive immune system. The innate immune system is the first to respond to pathogens and does not retain memory of previous responses. Innate immune responses are evolutionarily older than adaptive responses and elements of innate immunity can be found in all multicellular organisms. If a pathogen persists, the adaptive immune system will engage the pathogen with specificity and memory. Several components of the adaptive system including immunoglobulins (Igs), T cell receptors (TCR), and major histocompatibility complex (MHC), are assumed to have arisen in the first jawed vertebrates-the Gnathostomata. This review will discuss and compare components of both the innate and adaptive immune systems in Gnathostomes, particularly in Chondrichthyes (cartilaginous fish) and in Osteichthyes [bony fish: the Actinopterygii (ray-finned fish) and the Sarcopterygii (lobe-finned fish)]. While many elements of both the innate and adaptive immune systems are conserved within these species and with higher level vertebrates, some elements have marked differences. Components of the innate immune system covered here include physical barriers, such as the skin and gastrointestinal tract, cellular components, such as pattern recognition receptors and immune cells including macrophages and neutrophils, and humoral components, such as the complement system. Components of the adaptive system covered include the fundamental cells and molecules of adaptive immunity: B lymphocytes (B cells), T lymphocytes (T cells), immunoglobulins (Igs), and major histocompatibility complex (MHC). Comparative studies in fish such as those discussed here are essential for developing a comprehensive understanding of the evolution of the immune system.

Keywords: actinopterygii; adaptive immunity; chondrichthyes; innate immunity; sarcopterygii.

Figure 1

Schematic diagram of the evolution of jawed vertebrates and the immune system. Information sourced from multiple phylogenetic analyses (, , , –11). R: genome duplication event.

Figure 2

The three complement pathways with associated proteins. *Multiple C3 and/or C4 isoforms in some teleost and cartilaginous fish species. **Absence of mannose-binding lectin (MBL), ficolin, C1qA, and C1qC from genomes of any cartilaginous fish studied to date ***MASP2 transcript with no serine protease domain in hammerhead shark genome; MASP2 missing from elephant shark, little skate, and catshark genomes (–109).

Figure 3

Antibody diversity and isotypes are divergent in fish. (A) Arrangement of the heavy chain loci in bony fish and cartilaginous fish. V represents variable segments, D represents diversity segments, J represents joining segments and C represents constant domains. (B) Examples of the immunoglobulin isotypes in fish. Dark blue circles represent heavy chain domains, light blue circles represent light chain domains (–162). *IgM for lungfish only; no IgM in the coelacanth.

Figure 4

Schematic of the conventional TCR forms found in all Gnathostomes and NARTCR found in cartilaginous fish. Rectangles represent Ig super-family domains; V represent variable domains (white), C represents constant domains (purple) and NAR V represents extra variable domain in NARTCR (green). Modified from Criscitiello et al. (162), Roux et al. (253), and Criscitiello (254).