IMMUNITY AMONG DIFFERENT ANIMAL GROUPS

All animals, both invertebrates and verte­brates, possess innate immune defenses trig­gered by tissue damage or microbial invasion.

The acquired immune system evolved only after the emergence of jawless fishes; thus acquired immune mechanisms evolved only in the more recently evolved vertebrates (Tizard 2004).

Comparing Acquired Immunity in Mammals and Birds

Although both mammals and birds have com­plex immune systems, there are some important differences between them (Wakelin and Apanius 1997, Davison et al. 2008). Like mammals, birds are hosts for virtually every group of parasites, from viruses to helminths and arthropods (Wakelin and Apanius 1997). And like mam­mals, avian immune systems are characterized by a true two-component (B- and T-lymphocyte) system, including specific immunoglobulin antibody production, highly developed specific cellular immunity, and specific memory. How­ever, birds do not have lymph nodes, but have a central sinus that is the main lumen of a lym­phatic vessel, which contains germinal centers functionally equivalent to mammalian lymph nodes (Tizard 2004).

The thymus is the source of T-lymphocytes for both mammals and birds; it lies along the jugular vein in birds but overlies the heart in mammals. Rather than relying on bone mar­row for differentiation of B-cells, birds have a discrete organ, the bursa of Fabricius, located near the cloaca, that provides a microenvi­ronment for the differentiation and expan­sion of the B-cell compartment (Wakelin and Apanius 1997). The bursa also is the source of erythrocyte production in birds.

Based on the immunoglobulins of domestic galliform birds, there are three principal immu­noglobulin classes in birds: IgY (similar to IgG of mammals), IgM, and IgA (Tizard 2004). Thus far, IgE and IgD have not been reported in birds (Davison et al. 2008)

Avian IgM is homologous to the IgM from other vertebrate classes (Wakelin and Apanius 1997).

Immunoglobulin Y is the functional equiva­lent of IgG in birds, reptiles, and amphibians, and it is viewed as the ancestor to the uniquely mammalian antibodies IgG and IgE (Warr et al. 1995). Avian IgY differs from mammalian IgG in possessing an additional polypeptide domain (Wakelin and Apanius 1997). Because of the structural differences from mammalian IgG, many authors prefer to use the term IgY in place of avian IgG (Wakelin and Apanius 1997, Tizard 2004). Mammalian IgG has several subclasses, but this is not clearly established for avian IgY (Benedict and Yamaga 1976, Tizard 2004).

A functional analogue of mammalian IgA has been identified in galliform and columbi- form birds (Porter and Parry 1976, Goudswaard et al. 1977). However, the evolutionary rela­tionships between IgA of birds and those of mammals are not clear (Hadge and Ambrosius 1983, 1984).

Ducks, geese, and swans (Anseriformes) have some features distinct from other avian groups. The morphology of the bursa differs from other avian orders (von Rautenfield and Budras 1982). Some species of ducks have mul­tiple copies of the gene for antigen-binding sites of immunoglobulins, in contrast to the single copy found in other orders (McCormack et al. 1989). Anseriforms have a very uncommon form ofimmunoglobulin isotype called IgN that has only two of the four polypeptide domains that compose the IgY heavy chain (Magor et al. 1992, Tizard 2004). Thus, IgN has a lower molecular weight than IgY and reduced effec­tiveness for antibody activities such as agglu­tination and complement activation (Higgins 1989). Anseriforms secrete an IgM isotype into bile for protection of mucosal surfaces in the intestine (Ng and Higgins 1986), whereas galli- forms and columbiforms secrete an IgA isotype into bile, tracheal mucus, and tears (Wakelin and Apanius 1997).

Among galliform birds, newly hatched chicks have limited but detectable innate and acquired immune responses (Seto and Hender­son 1967). Immunoglobulin Y antibodies are transported into the yolk and provide protection for chicks for the first two weeks of life until the immunoglobulins are catabolized (Rose et al. 1974). The qualitative and quantitative expres­sions of acquired immune responses increase with the growth of galliform chicks and pla­teaus between 6 and 12 weeks (Rose 1967, Solomon 1968, Lawrence et al. 1981, Suresh et al. 1993).

Acquired Immunity in Reptiles

Immunoglobulins first appeared at the level of jawless fishes. Distinctive T- and B-cells first are seen among amphibians (Sell 1996). Rep­tiles have regulatory T-cells, cells with surface immunoglobulin and lymphoid organs that resemble those of mammals (Sell 1996).

Primitive lymph nodules surround the aorta, vena cava, and jugular veins. Lympho­cytes and plasma cells are found in the nodules in the intestinal wall, and some lymphocytes are found in the kidneys of reptiles (Tizard 2004). In most reptiles, a bursa-like organ is present (Black 2002). In most reptiles also, the thymus develops from pharyngeal pouches and is structurally similar to the thymus of other vertebrate classes (Tizard 2004); however, no thymus has been described for alligators and crocodiles (Black 2002).

Among turtles, the IgM is comparable to mammalian IgM in size, chain structure, and carbohydrate content (Tizard 2002). Turtles and lizards can mount both primary and secondary antibody responses, with IgM produced in the pri­mary response and IgY produced in the second­ary response (Tizard 2004). There is evidence of cell-mediated immune responses such as mixed lymphocyte reactions and delayed hypersensitiv­ity reactions among reptiles (Tizard 2004).

Immunity in Amphibians

Resistance to pathogens involves both an innate immune system and an acquired immune sys­tem (Carey et al. 1999). A first defense against pathogens found in the skin and digestive tract of amphibians consists of small, basic antimi­crobial peptides active against bacteria, yeasts, and fungi (Jacob and Zasloff 1994, Nicolas and Mor 1995, Rollins-Smith et al. 2002). Like other vertebrates, amphibians have phagocytic cells such as macrophages and neutrophils, a comple­ment system, and natural killer (NK) cells (Carey et al. 1999). Innate immunity is perceived to be an important part of amphibian defenses (Carey et al. 1999, Richmond et al. 2009).

Acquired immunity has not been studied in many amphibians. Based on the African clawed frog (Xenopus laevis) and the axolotl (Ambystoma mexicanum), the acquired immune system of amphibians appears to have many similarities to that of mammals (Carey et al. 1999). These include B- and T-lymphocytes (Bleicher and Cohen 1981), several types of immunoglobulins (Carey et al. 1999), cyto­kines (Haynes and Cohen 1993), and major histocompatibility complex (MHC) class I and class II genes (Flajnik and DuPasquier 1990). Xenopus laevis lacks lymph nodes and lympho­poietic bone marrow, but does have a thymus and spleen (Carey et al. 1999). Interestingly, salamanders have many of the same immune features described for frogs and toads, but often have a weaker acquired immune response; the reasons are not clear (Carey et al. 1999).

Immunity in Arthropods

Because of their role as disease vectors to ver­tebrates, there is also some interest in arthro­pod immunity. Among their initial defenses, arthropods have a hard chitinous covering that is shed periodically; many also have a high (alkaline) pH in their guts as well as a number of antibacterial substances that inhibit infection by bacteria (Heimpel and Harshbarger 1965).

Arthropods generally protect themselves against invasion by processes of phagocytosis, some antibody-like molecules, and by physical barriers (Tizard 2002). Several types of phago­cytic cells occur in invertebrates, including hemocytes and coelomocytes (Heimpel and Harshbarger 1965). These cells function simi­larly to mammalian phagocytes and undergo chemotaxis, adherence, and ingestion, as well as digestion of foreign materials; they also con­tain proteases (Tizard 2002). Toll-like receptors have been found in all multicellular organisms examined to date (O'Neill 2004).

Arthropods possess a family of enzymes that, when activated, can generate a cascade of proteases leading to the production of phenoloxidase, an enzyme that binds to for­eign surfaces and generates melanin around sites where immune defense reactions occur (Tizard 2002). Phenoloxidase enhances phago­cytosis and is bactericidal and fungicidal (Tizard 2002).

Some insects produce proteins that slow bacterial growth or lyse bacteria. Some insects also induce proteins that mimic antibody mole­cules. However, little is known about the mech­anisms of these antibacterial proteins (Tizard 2002). Although plague bacteria (Yersinia pes- tis) can remain in fleas for well over a year in some circumstances, there also is evidence that bacteriophages in the intestines of fleas lyse the microbes and can free 60-70% of the infected fleas from plague bacilli in one to three days (Pavlovski 1966).

Almost all bacteria are cleared from an insect by phagocytosis and melanization, a unique immune defense mechanism primar­ily of insects involving the production of mela­nin, a brown-black pigment that accompanies innate immune responses against several microorganisms (Haine et al. 2008, Schneider and Chambers 2008). Antimicrobial proteins likely remove the bacteria remaining after these more general defensive mechanisms have finished, and this may help explain why bacteria generally have not been successful in developing resistance to arthropod peptides.