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.

Warming at the population level: Effects on age structure, density, and generation cycles

“…All time series also show peaks at frequencies close to zero, which arise from the multigeneration cycles which are apparent in the time series in addition to the generation cycles other and pupae (Cameron et al, 2007;Reed, 1998). At 30°C, P. interpunctella egg-to-adult survival is reduced and overall fecundity is lower (Laughton et al, 2017;Parrett & Knell, 2018). This reduction in recruitment means that competition between larvae is likely to be reduced, which is consistent with the more even age distributions of larvae found at 30°C.…”

“…When resources are scarce the larger 4th and 5th instar larvae not only outcompete smaller larvae, but will also cannibalize eggs, smaller larvae, each other and pupae (Cameron et al, ; Reed, ). At 30°C, P. interpunctella egg‐to‐adult survival is reduced and overall fecundity is lower (Laughton et al, ; Parrett & Knell, ). This reduction in recruitment means that competition between larvae is likely to be reduced, which is consistent with the more even age distributions of larvae found at 30°C.…”

“…In the case of P. interpunctella, there has been a considerable amount of research on the life‐history effects of temperature, summarized in Table . Work on the strain used in these experiments found that increasing temperature from 27°C (the standard laboratory rearing temperature) to 30°C reduces the egg‐to‐eclosion period by 2–3 days and adult lifespan by 2.5 days, with 50% of unmated females surviving for 12.5 days at 27°C and 10 days at 30°C (Laughton, O'Connor, & Knell, ), suggesting that generation cycles should become shorter with increasing temperature. This assumes that other temperature effects on life‐history characters in P. interpunctella do not influence the behavior of the populations, however, and it is possible that changes in factors like recruitment could override this: Lifetime fecundity of females is reduced by 20%–25% by an increase from 27 to 30°C (Laughton et al, ).…”

“…Work on the strain used in these experiments found that increasing temperature from 27°C (the standard laboratory rearing temperature) to 30°C reduces the egg‐to‐eclosion period by 2–3 days and adult lifespan by 2.5 days, with 50% of unmated females surviving for 12.5 days at 27°C and 10 days at 30°C (Laughton, O'Connor, & Knell, ), suggesting that generation cycles should become shorter with increasing temperature. This assumes that other temperature effects on life‐history characters in P. interpunctella do not influence the behavior of the populations, however, and it is possible that changes in factors like recruitment could override this: Lifetime fecundity of females is reduced by 20%–25% by an increase from 27 to 30°C (Laughton et al, ). Increasing temperature has also been found to have a pronounced effect on egg‐to‐adult survival in P. interpunctella , with the proportion of eggs leading to eclosing adults changing from roughly 60% at 27°C to between 20% and 30% at 33°C (Parrett & Knell, ).…”

“…24° females lay consistent numbers of eggs per day throughout their lifespan. At 26, 28, and 30° females lay most of their eggs in the first few days of adulthoodLaughton et al (2017) …”