Compensating for delayed hatching reduces offspring immune response and increases life‐history costs

Abstract

Organisms are exposed to multiple sources of stress in nature. When confronted with a stressful period affecting growth and development, compensatory responses allow the restoration of individual fitness, providing an important buffering mechanism against climatic and other environmental variability. However, tradeoffs between increased growth/development and other physiological traits are predicted to prevent these high growth and development rates from becoming constitutive. Here, we investigated how compensatory responses in growth and development affect immune responses. By using low temperature to stop embryonic development, we exposed moor frog Rana arvalis tadpoles to two levels of time‐constraints: non‐delayed hatching and 12‐day delayed hatching. In a common garden experiment, we recorded larval growth and development, as well as their immune response, measured as the inflammatory reaction after the injection of phytohaemagglutinin (PHA). Tadpoles originating from delayed hatching treatments had a lower immune response to PHA challenge than those from the non‐delayed hatching treatment. In general, tadpoles from the delayed hatching treatment reached metamorphosis faster and at a smaller size than control tadpoles. However, immune‐challenged tadpoles were not able to accelerate their development in response to delayed hatching. Our results indicate that 1) the innate immune response can be reduced in organisms undergoing compensatory developmental responses in growth and development and 2) compensatory capacity can be reduced when organisms are immunologically challenged. These dual findings reveal the complexity of handling multiple stressors and highlight the importance of examining the costs and limits of mounting an immune response in the context of increasing phenological instability ascribed to climate change.

The effects of different cold‐temperature regimes on development, growth, and susceptibility to an abiotic and biotic stressor

“…Both cold‐temperature regimes caused a consistent reduction in tadpole mass compared to the control. Contrary to our findings, past studies show that cold‐delayed tadpoles can induce compensatory growth responses (Murillo‐Rincón, Laurila, & Orizaola, ; Orizaola et al, ; Orizaola, Richter‐Boix, & Laurila, ). In our study, we did not observe the induction of compensatory growth responses, as the tadpoles exposed to both cold treatments were consistently smaller over the course of the study.…”

“…Finally, we investigated the influence of different cold‐temperature regimes on wood frog susceptibility to parasites. We hypothesized that tadpoles exposed to cold temperatures would exhibit higher infection loads because immune function has been demonstrated to be compromised in developmentally delayed tadpoles (Murillo‐Rincón et al, ). Similarly, Rohr and Raffel () and Raffel et al () demonstrate that temperature variability increased host susceptibility to infection by the fungal parasite Batrachochytrium dendrobatidis .…”

Metabolic costs of altered growth trajectories across life transitions in amphibians

“…Here, using the common frog ( Rana temporaria ) as a model species, we examined the metabolic changes induced by altering growth trajectories early in life, by measuring oxidative stress, corticosterone levels and telomere length across the entire larval development. In a laboratory experiment, we exposed frog embryos to cold conditions that intended to mimic a period of cold weather shortly after laying, stopping development and inducing a delay in hatching (Murillo‐Rincón et al, ; Orizaola et al, ). This cold period is representative of a ‘false spring’ scenario, in which weather conditions fluctuate and winter temperatures come back after breeding, something expected to occur more and more often as a consequence of climate change (Chamberlain, Cook, García de Cortázar‐Atauri, & Wolkowich, ).…”

Photoperiodic cues regulate phenological carry‐over effects in an herbivorous insect

“…In a recent study in the moor frog, Orizaola et al . show that compensatory growth in response to early ontogeny conditions influences immune response later in life (Murillo‐Rincón, Laurila, & Orizaola, ). Similar results were found in damselflies (De Block & Stoks, ).…”