Transmissible cancer influences immune gene expression in an endangered marsupial, the Tasmanian devil (Sarcophilus harrisii)

Abstract

Understanding the effects of wildlife diseases on populations requires insight into local environmental conditions, host defence mechanisms, host life-history trade-offs, pathogen population dynamics, and their interactions. The survival of Tasmanian devils (Sarcophilus harrisii) is challenged by a novel, fitness limiting pathogen, Tasmanian devil facial tumour disease (DFTD), a clonally transmissible, contagious cancer. In order to understand the devils' capacity to respond to DFTD, it is crucial to gain information on factors influencing the devils' immune system. By using RT-qPCR, we investigated how DFTD infection in association with intrinsic (sex and age) and environmental (season) factors influences the expression of 10 immune genes in Tasmanian devil blood. Our study showed that the expression of immune genes (both innate and adaptive) differed across seasons, a pattern that was altered when infected with DFTD. The expression of immunogbulins IgE and IgM:IgG showed downregulation in colder months in DFTD infected animals. We also observed strong positive association between the expression of an innate immune gene, CD16, and DFTD infection. Our results demonstrate that sampling across seasons, age groups and environmental conditions are beneficial when deciphering the complex ecoevolutionary interactions of not only conventional host-parasite systems, but also of host and diseases with high mortality rates, such as transmissible cancers.

Keywords: cancer; conservation physiology; host-parasite interactions; immune system; life history trade-off.

FIGURE 1

Correlation matrix displaying pearson correlation coeffients calculated between immune gene expression profiles in Tasmanian devils. Matrix is ordered by similarity. Pearson's correlation coefficients are printed in matrix, strength of correlation is represented visually by circle size and colour. Larger circles, higher correlation coefficients (stronger linear relationship); smaller circles, lower correlation coefficients (weaker linear relationship); red, positive correlation; blue, negative correlation

FIGURE 2

Heatmap as a visual representation of the model estimate (slope) for explanatory variables influencing gene expression profiles in Tasmanian devils, across all genes. For categorical explanatory variables the intercepts are: Season, summer; DFTD, healthy; Sex, female. The specific colour shows the direction of the effect blue, negative slope; red, positive slope. The intensity of colour illustrates the strength of the effect. p‐values calculated from models are indicated as: *** <.001, ** <.01, * <.05, . <.1

FIGURE 3

(a) Marginal means effects of DFTD infection, red dots are raw data. (b) Marginal means effects of interactions with DFTD infection and sex for each gene, red, healthy animals; blue, visibly DFTD affected animals. (c) Marginal means effects of interactions with DFTD infection and season for each gene. Black, healthy animals; orange, visibly DFTD affected animals. 95% confidence intervals are displayed. Only statistically significant results are graphed

FIGURE 4

Marginal means effects of season, 95% confidence intervals are displayed. Only statistically significant results are graphed. Marginal means: The effect of a specific explanatory variable, accounting for all other variables in the model, Raw data: light blue dots

FIGURE 5

Marginal means effects of age, black dots are raw data. 95% confidence intervals are shown. Only statistically significant results are graphed