Thermal sensitivity of immune function: evidence against a generalist-specialist trade-off among endothermic and ectothermic vertebrates

Michael W. Butler; Zachary R. Stahlschmidt; Daniel R. Ardia; Scott Davies; Jon Davis; Louis J. Guillette; Nicholas Johnson; Stephen D. McCormick; Kevin J. McGraw; Dale F. DeNardo

doi:10.1086/670191

USGS · 70047219

Thermal sensitivity of immune function: evidence against a generalist-specialist trade-off among endothermic and ectothermic vertebrates

Michael W. Butler·Zachary R. Stahlschmidt·Daniel R. Ardia·Scott Davies·Jon Davis·Louis J. Guillette·Nicholas Johnson·Stephen D. McCormick·Kevin J. McGraw·Dale F. DeNardo

View original source ↗Export metadata ↓

Abstract

Animal body temperature (Tbody) varies over daily and annual cycles, affecting multiple aspects of biological performance in both endothermic and ectothermic animals. Yet a comprehensive comparison of thermal performance among animals varying in Tbody (mean and variance) and heat production is lacking. Thus, we examined the thermal sensitivity of immune function (a crucial fitness determinant) in Vertebrata, a group encompassing species of varying thermal biology. Specifically, we investigated temperature-related variation in two innate immune performance metrics, hemagglutination and hemolysis, for 13 species across all seven major vertebrate clades. Agglutination and lysis were temperature dependent and were more strongly related to the thermal biology of species (e.g., mean Tbody) than to the phylogenetic relatedness of species, although these relationships were complex and frequently surprising (e.g., heterotherms did not exhibit broader thermal performance curves than homeotherms). Agglutination and lysis performance were positively correlated within species, except in taxa that produce squalamine, a steroidal antibiotic that does not lyse red blood cells. Interestingly, we found the antithesis of a generalist-specialist trade-off: species with broader temperature ranges of immune performance also had higher peak performance levels. In sum, we have uncovered thermal sensitivity of immune performance in both endotherms and ectotherms, highlighting the role that temperature and life history play in immune function across Vertebrata.

Explore related subjects

American Naturalist Article

Keep this discovery

Explore connections, maps & timelines

BibTeX RIS

Michael W. Butler, Zachary R. Stahlschmidt, Daniel R. Ardia, Scott Davies, Jon Davis, Louis J. Guillette, Nicholas Johnson, Stephen D. McCormick, Kevin J. McGraw, Dale F. DeNardo. 2013. Thermal sensitivity of immune function: evidence against a generalist-specialist trade-off among endothermic and ectothermic vertebrates. https://doi.org/10.1086/670191

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related USGS reports

USGS2021

Infection status as the basis for habitat choices in a wild amphibian

Animals challenged with disease may select specific habitat conditions that help prevent or reduce infection. Whereas preinfection avoidance of habitats with a high risk of disease exposure has been documented in both captive and free-ranging animals, evidence of switching habitats after infection to support the clearing of the infection is limited to laboratory experiments. The extent to which wild animals proximately modify habitat choices in response to infection status thus remains unclear. We investigated preinfection behavioral avoidance and postinfection habitat switching using wild, radio-tracked boreal toads ( Anaxyrus boreas boreas ) in a population challenged with Batrachochytrium dendrobatidis ( Bd ), a pathogenic fungus responsible for a catastrophic panzootic affecting hundreds of amphibian species worldwide. Boreal toads did not preemptively avoid microhabitats with conditions conducive to Bd growth. Infected individuals, however, selected warmer, more open habitats, which were associated with elevated body temperature and the subsequent clearing of infection. Our results suggest that disease can comprise an important selective pressure on animal habitat and space use. Habitat selection models, therefore, may be greatly improved by including variables that quantify infection risk and/or the infection status of individuals through time.

Wyoming↗

USGS2020

Quantifying the contribution of habitats and pathways to a spatially structured population facing environmental change

The consequences of environmental disturbance and management are difficult to quantify for spatially structured populations because changes in one location carry through to other areas as a result of species movement. We develop a metric, G , for measuring the contribution of a habitat or pathway to network-wide population growth rate in the face of environmental change. This metric is different from other contribution metrics, as it quantifies effects of modifying vital rates for habitats and pathways in perturbation experiments. Perturbation treatments may range from small degradation or enhancement to complete habitat or pathway removal. We demonstrate the metric using a simple metapopulation example and a case study of eastern monarch butterflies. For the monarch case study, the magnitude of environmental change influences the ordering of node contribution. We find that habitats within which all individuals reside during one season are the most important to short-term network growth under complete removal scenarios, whereas the central breeding region contributes most to population growth over all but the strongest disturbances. The metric G provides for more efficient management interventions that proactively mitigate impacts of expected disturbances to spatially structured populations. use changes in one location carry through to other areas due to species movement. We develop a metric, G, for measuring the contribution of a habitat or pathway to network-wide population growth rate in the face of environmental change. This metric is different than other contribution metrics as it quantifies effects of modifying vital rates for habitats and pathways in perturbation experiments. Perturbation treatments may range from small degradation or enhancement to complete habitat or pathway removal. We demonstrate the metric using a simple metapopulation example and a case study of eastern monarch butterflies. For the monarch case study, the magnitude of environmental change influences ordering of node contribution. We find that habitats through which all migrants flow are the most important to short-term network growth under complete-removal scenarios. The metric G provides for more efficient management interventions that proactively mitigate impacts of expected disturbances to spatially structured populations.

American Naturalist↗

USGS2019

Brood size affects future reproduction in a long-lived bird with precocial young

Estimation of trade-offs between current reproduction and future survival and fecundity of long-lived vertebrates is essential to understanding factors that shape optimal reproductive investment. Black brant geese (Branta bernicla nigricans) fledge more goslings, on average, when their broods are experimentally enlarged to be greater than the most common clutch size of four eggs. Thus, we hypothesized that the lesser frequency of brant clutches exceeding four eggs results, at least partially, from a future reduction in survival, breeding probability, or clutch size for females tending larger broods. We used an eight-year mark-recapture dataset (Barker robust design) with five years of clutch and brood manipulations to estimate long-term consequences of reproductive decisions in brant. We did not find evidence of a trade-off between reproductive effort and true survival or future initiation date and clutch size. Rather, future breeding probability was maximized (0.92 ± 0.03 [se]) for manipulated females tending broods of four goslings and lower for females tending smaller (one gosling; 0.63 ± 0.09 [se]) or larger broods (seven goslings; 0.52 ± 0.15 [se]). Our results suggest that demographic trade-offs for female brant tending large broods may reduce the fitness value of clutches larger than four and, therefore, contribute to the paucity of larger clutches. The lack of a trade-off between reproductive effort and survival provides evidence that survival, to which fitness is most sensitive in long-lived animals, is buffered against temporal variation in brant.

American Naturalist↗