Adaptive developmental plasticity and hormetic effects in the zebra finch (Taeniopygia castanotis)

Abstract

Stressors experienced during development can have persisting detrimental effects on an individual’s phenotype, as well as indirect effects on the phenotype of offspring. However, developmental stressors can also be beneficial depending on the timing, intensity, and duration of the stressor. Stressor exposure during development may act instructively, inducing changes in phenotype that make the organism, and sometimes their offspring, more suited for the potential poor environmental conditions they will experience in adulthood. This is known as adaptive developmental plasticity. Although it has the potential to influence population dynamics and evolutionary change, research examining adaptive developmental plasticity in endothermic vertebrates such as birds is limited. Moreso, we have a poor understanding of the underlying physiological changes mediating these effects, the potential trade-offs with key fitness-related traits, and how these relationships vary due to the adult environment. I address these gaps through experimental studies in the laboratory utilizing zebra finches (Taeniopygia castanotis). We exposed the finches to a prolonged mild heat (38 °C) conditioning or control (22 °C) treatment during juvenile development. As adults, the finches were exposed to a high heat stressor (42 °C) or control (22 °C) treatment in a 2x2 factorial design. We measured multiple cellular and life-history traits to determine 1) whether exposure to the mild heat conditioning during development induces an adaptive phenotypic adjustment, giving the finches an increased ability to buffer the negative effects of the high heat stressor as adults, 2) what physiological changes mediate this potential adaptive plasticity, 3) the potential costs and trade-offs between traits associated with the phenotypic change in stressful and benign environments. Furthermore, we determined whether the mild heat conditioning induced adaptive intergenerational plasticity, preparing the offspring of the finches to better cope with elevated ambient temperatures. In Chapter 2, we saw that exposure to the mild heat conditioning induced a hormetic effect, preventing an increase in egg laying latency in adulthood after exposure to the high heat stressor. However, we also saw that exposure to either the conditioning as juveniles and/or the high heat stressor as adults had a stimulatory effect on the clutch viability of female finches. Surprisingly, there was seemingly no negative impacts of the high heat stressor on immune function (measured via wound healing) or several female reproductive parameters. However, there seemed to be a potential cost of the phenotypic change induced by the mild heat conditioning, but only when their adult environment did not “match”. The female finches exposed to the mild heat conditioning as juveniles and the control treatment as adults had wounds that took longer to heal than those exposed to the high heat stressor as adults, regardless of whether they were exposed to the conditioning during development. These results indicate the potential for the presence of trade-offs between traits or a shift in life-history strategy. In Chapters 3 and 4, we investigated whether exposure to the mild heat conditioning during development resulted in adaptive variation in adult antioxidant enzymes and heat-shock protein expression, reducing oxidative damage when exposed to the high heat stressor as adults. Moreso, we examined the relationships between the oxidative measurements and beak color - a sexually selected trait - to determine if the physiological changes induced trade-offs with, or buffered negative effects of heat stress on beak color. We saw that conditioned males had higher beak saturation and lower brightness in adulthood, but the response to the high heat stressor varied. When exposed to the high heat stressor as adults, conditioned males had higher levels of superoxide dismutase 1 & 2 antioxidant enzymes and reduced levels of HSP90 and HSP60 in the testes, as well as lower levels of cellular lipid oxidative damage in the liver, indicating an adaptive phenotypic change. In Chapter 5, we investigated whether altered responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis resulting from the mild heat conditioning acts as a mediator of adaptive developmental plasticity, and the association with DNA damage and survival when exposed to the high heat stressor as adults. Conditioned female finches had higher baseline DNA damage levels and body masses than juvenile control females, as well as lower corticosterone levels following the adult treatment. However, once again we saw a cost when there was a mismatch between the juvenile and adult environment, as conditioned females exhibited reduced survival if they were not also exposed to the high heat stressor as adults. In Chapter 6, we investigated whether maternal exposure to the mild heat conditioning during development would induce a form of intergenerational phenotypic plasticity known as maternal effects, and how the direction of this effect would be influenced by the maternal adult environment. Moreso, we determined whether the conditioning would act as an anticipatory maternal effect, resulting in offspring that are better suited to cope with high incubation temperatures as embryos. We found that embryos from conditioned mothers exhibited reduced water loss, longer development times, and heavier pectoralis muscles as hatchlings, when incubated at high incubation temperatures, compared to offspring from control mothers. The conditioned mothers that were also exposed to the high heat stressor as adults laid eggs with a higher density of shell pores, and embryos with lower heart rates during development. However, embryos from these conditioned and heat stressed mothers had reduced survival at control incubation temperatures, once again indicating potential costs when the future environment does not “match” the environment which induced the phenotypic change. The chapters of this dissertation demonstrate that mild developmental stressors can have beneficial effects on phenotype in zebra finches, however, the effects are clearly context dependent. The adaptiveness depends on both the trait being measured and the matching between the early life and adult environment of the finches. Mild developmental stressors can clearly have persisting impacts on a fitness-related traits at multiple biological levels, and research should integrate this knowledge when determining how populations will respond to rapid environmental change.