Responses to a warming world: Integrating life history, immune investment, and pathogen resistance in a model insect species

Abstract

Environmental temperature has important effects on the physiology and life history of ectothermic animals, including investment in the immune system and the infectious capacity of pathogens. Numerous studies have examined individual components of these complex systems, but little is known about how they integrate when animals are exposed to different temperatures. Here, we use the Indian meal moth (Plodia interpunctella) to understand how immune investment and disease resistance react and potentially trade-off with other life-history traits. We recorded life-history (development time, survival, fecundity, and body size) and immunity (hemocyte counts, phenoloxidase activity) measures and tested resistance to bacterial (E. coli) and viral (Plodia interpunctella granulosis virus) infection at five temperatures (20-30°C). While development time, lifespan, and size decreased with temperature as expected, moths exhibited different reproductive strategies in response to small changes in temperature. At cooler temperatures, oviposition rates were low but tended to increase toward the end of life, whereas warmer temperatures promoted initially high oviposition rates that rapidly declined after the first few days of adult life. Although warmer temperatures were associated with strong investment in early reproduction, there was no evidence of an associated trade-off with immune investment. Phenoloxidase activity increased most at cooler temperatures before plateauing, while hemocyte counts increased linearly with temperature. Resistance to bacterial challenge displayed a complex pattern, whereas survival after a viral challenge increased with rearing temperature. These results demonstrate that different immune system components and different pathogens can respond in distinct ways to changes in temperature. Overall, these data highlight the scope for significant changes in immunity, disease resistance, and host-parasite population dynamics to arise from small, biologically relevant changes to environmental temperature. In light of global warming, understanding these complex interactions is vital for predicting the potential impact of insect disease vectors and crop pests on public health and food security.

Keywords: Plodia interpunctella; defense; ecological immunology; global warming; hemocyte; phenoloxidase; trade‐off.

Figure 1

Temperature effects on Plodia developmental time showing both egg‐to‐pupa time and pupal duration. The full bar is therefore the egg‐to‐eclosion time. Error bars are ±1 SEM. The line shows the predicted values from the fitted quadratic model

Figure 2

Temperature effects on the wing length (a proxy for adult body size). Error bars are ±1 SEM. Fitted lines show the predicted values from the fitted quadratic model

Figure 3

Survival of mated and unmated female moths at different temperatures. Solid lines indicate unmated moths and dashed lines mated ones. Color fills show the differences between mated and unmated at different temperatures. NB 27° treatment not shown for clarity, but it is intermediate between 24 and 30°C

Figure 4

Number of eggs laid per 48 hr plus the fitted smoothers from the GAMM for each temperature. At 20°, the moths live for a long time and produce a few eggs every day. The moths at 22° have a similarly low oviposition rate but toward the end of their lives some of them increase the number of eggs laid (NB some of the 20° moths did this as well but some did not). Once the temperature reaches 24° and up oviposition is mostly early on in the animals’ lives, with large numbers of eggs laid in the first few days

Figure 5

Temperature effects on hemocyte count. The bars show means and 95% confidence intervals for square‐root hemocyte count for each temperature treatment. The fitted line shows the predicted values from the model

Figure 6

Phenoloxidase activity plotted against temperature. The line indicates predicted values from the fitted model. Error bars are 95% confidence intervals

Figure 7

Square‐root PO activity plotted against square‐root hemocyte count. The line is for illustrative purposes only and shows the results of a simple linear regression through the data

Figure 8

Temperature effects on bacterial clearance. The bars show means and 95% confidence intervals for log bacterial counts for each temperature treatment. The fitted line shows the predicted values from the fitted cubic model

Figure 9

Ability of Plodia to resist infection with PiGV under two different temperature regimes. Moths experienced either a constant pre‐ and postinfection temperature or were raised at 26°C and only separated into temperature treatment groups after being dosed with PiGV. Virus resistance declines with temperature, but only when temperatures before and after infection are both manipulated. When only the temperatures after infection are manipulated, there is little effect of temperature. Lines indicate predicted values from the fitted model. Error bars are ±1 binomial SEM