Metamorphosis and the amphibian immune system

Abstract

Studies of the ontogeny of immunity in a limited number of representative amphibians have shown that while the immune systems of the larval forms are competent to defend against potential pathogens in the temporary ponds they inhabit, they are not equivalent to the mature immune systems that develop after metamorphosis. Metamorphosis is a critical time of transition when increased concentrations of metamorphic hormones, principally thyroid hormones (TH) and corticosteroid hormones (CH), orchestrate the loss or reorganization of many tissues and organ systems, including the immune system. Immune system reorganization may serve to eliminate unnecessary lymphocytes that could be destructive if they recognized newly emerging adult-specific antigens on the adult tissues. Increased corticosteroids during metamorphosis appear to induce apoptosis of susceptible lymphocytes. This cell death can be inhibited in vitro or in vivo by the corticosteroid receptor antagonist, RU486. A coordinate increase in both TH and CH at metamorphosis may be common to all amphibians that undergo metamorphosis. Current evidence suggests that the central hypothalamic mediator that induces pituitary production of both thyroid-stimulating hormone and adrenocorticotropic hormone in larval amphibians is corticotropin-releasing hormone. Most amphibians probably survive the temporary immunosuppression associated with metamorphosis with no deleterious effects. However, it is hypothesized that if environmental stressors result in the induction of metamorphosis at a less than optimal body size and state of immune maturation, the immune system destruction would be more significant, and the amphibians could be at greater risk of infection and death.

SUSCEPTIBILITY TO THE AMPHIBIAN CHYTRID FUNGUS VARIES WITH ONTOGENY IN THE DIRECT-DEVELOPING FROG,ELEUTHERODACTYLUS COQUI

“…The ontogeny of the amphibian immune system has been studied in only one anuran, Xenopus laevis, a species with larval development (Rollins-Smith 1998). Innate immune responses, such as secretion of antimicrobial peptides, are one of several factors known to influence amphibian susceptibility (Rollins-Smith et al 2011); other factors include symbiotic skin bacteria that inhibit Bd (Harris et al 2006), microhabitat preferences (Brem andLips 2008), and thermoregulatory behavior (Richards-Zawacki 2010).…”

Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas)

“…Larval amphibians (for example, tadpoles) have innate immune cells in the form of lymphocytes, which decline during metamorphosis and then reestablish postmetamorphosis (Rollins-Smith, 1998). Many immune cells begin forming in organs absent in tadpoles, such as the kidney and bone marrow (Rollins-Smith, 1998). The adaptive immune functions increase significantly after metamorphosis, including MHC class 1 and 2 antigen recognition domains (Rollins-Smith, 1998).…”

“…Many immune cells begin forming in organs absent in tadpoles, such as the kidney and bone marrow (Rollins-Smith, 1998). The adaptive immune functions increase significantly after metamorphosis, including MHC class 1 and 2 antigen recognition domains (Rollins-Smith, 1998). Consequently, skin-associated microbial communities and the innate immune system may serve as the primary lines of defense against pathogens for larval amphibians before the adaptive immune system is fully functional.…”

“…For amphibians with biphasic life history strategies, the immune system is restructured during metamorphosis. Larval amphibians (for example, tadpoles) have innate immune cells in the form of lymphocytes, which decline during metamorphosis and then reestablish postmetamorphosis (Rollins-Smith, 1998). Many immune cells begin forming in organs absent in tadpoles, such as the kidney and bone marrow (Rollins-Smith, 1998).…”

“…Driven by the innate immune system in early life stages, defensive glands in the skin produce antimicrobial peptides, alkaloids and lysozymes, which limit the growth of some bacterial taxa and promote growth of others . Post metamorphosis, amphibians reorganize the adaptive immune system, which can mount the production of B and T lymphocytes and antigen-specific antibodies that can distinguish beneficial microbiota and self from nonself (Rollins-Smith, 1998). To determine which, if any role skin microbial communities play in these transitions in the immune system during development, we must sample these communities across developmental stages.…”