Immunocompetence in a long‐lived ectothermic vertebrate is temperature dependent but shows no decline in older adults

Abstract

Summary Temperature affects nearly all aspects of the physiology of ectotherms, including their ability to mount an immune response. Typically, the ectothermic vertebrate immune system can respond over a wide range of temperatures, but there is a species‐specific temperature at which responses are strongest, with impaired responses above and below this threshold. In long‐lived ectotherms, ageing could also influence the ability to respond to temperature changes as immunosenecence, the functional decrease in immune function with age, is widely reported. This study examined the effects of the interaction between temperature and age on B‐cell function in a long‐lived reptile, the red‐eared slider turtle, Trachemys scripta. B cells in this species have previously been shown to have two main functions, phagocytosis and antibody production. Adult turtles were trapped and blood samples taken. Because sliders grow throughout their lifetime, plastron length was used as a proxy for age. Leucocytes were isolated and used in either an ELISpot assay to examine their ability to produce antibodies spontaneously or when stimulated, or used in a phagocytic assay. The ELISpot and phagocytic assays were conducted over a range of biologically relevant temperatures. We found no interaction between age and temperature on any measure of B‐cell function. In all cases there was a significant effect of temperature, with impaired function at temperatures below 29 °C, but no impairment of function at higher temperatures. We also found little evidence of immunosenescence in any response. This study provides insight into the thermal biology of B‐cell function in sliders and provides an interesting connection between immunology, behaviour and ecology in this long‐lived turtle. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12867/suppinfo is available for this article.

Clinical Manifestation and Molecular Characterization of a Novel Member of the Nannizziopsiaceae in a Pulmonary Granuloma From a Galapagos Tortoise (Chelonoidis nigra)

“…Palm Beach, 45 km north of Boca Raton, has average temperatures of 28 • C during the hottest month of the year, and 18.6 • C during the coolest month of the year (https://en.climate-data.org). Temperatures outside the range for which ectotherms are adapted to can be expected to result in suboptimal immune function (30,31).…”

Eco-immunology in the cold: the role of immunity in shaping the overwintering survival of ectotherms

“…The ectotherm immune system relies on the temperature-dependent activity of enzymes and cells, and immune performance is therefore also constrained by temperature. Although the number of studies on the thermal performance of the ectotherm immune system is limited, immune activity generally conforms to a classic thermal performance curve and operates over a wide range of temperatures (Butler et al, 2013;Ferguson et al, 2016;Graham et al, 2017;Murdock et al, 2012;Zimmerman et al, 2017).…”

Relationships between parasitic infection and natural antibodies, age, and sex in a long‐lived vertebrate

“…Studies on sliders have found characteristics of a NAb response, including an age‐related increase in both total antibody levels and antigen‐specific antibody levels and an ability to bind to novel antigens (Zimmerman, Paitz, Vogel, & Bowden, , ). Further, the B cells in the slider turtle are believed to be similar to the B‐1 subset, which maintain function with age (Zimmerman et al., , ). However, it is unknown how the slider uses these NAbs in response to potential pathogens.…”