Evolutionary adaptation and constraint in the decoupling of immune responses across life stages

Vanderbilt University, Nashville TN

Investigators

Abstract

Whether an organism is a plant, insect, or human, its immune system must contend with exposure to parasites many times in its life. Immune responses cost energy, cause damage to self, and can interfere with development. Thus, young organisms may benefit, in terms of health and fitness, from a different level of immunity than older organisms. Metamorphic animals like insects have an advantage over humans and other continuously developing animals because they can remodel their bodies – and immune systems – as they age from juveniles to adults. This project uses experimental, genomics, and computational approaches in the flour beetle Tribolium castaneum to test the hypothesis that metamorphosis makes it easier to evolve different immune responses in different life stages, but only if the immune response does not impact development. This project will shed light on a fundamental question in immunology: why is there so much variation between individuals of different ages in how sick they get from infection? At the same time, it will help to explain why some species have evolved metamorphosis while others have not. The project will train several graduate and undergraduate students in computational and genomic techniques and provide educational outreach opportunities to understand how evolution affects agriculturally important insects. To test the hypothesis that metamorphosis enables selection to act relatively independently on the genetic basis of immune system regulation in different life stages unless the immune response is under developmental constraint, the researchers will undertake three objectives: 1) experimental evolution of stage-specific resistance against parasites targeted by immune pathways that vary in their effect on development in an emerging model insect (the flour beetle Tribolium castaneum), 2) quantification of natural variation in immune responses across life stages and populations to disentangle the contributions of development and local adaptation to immune system variation, and 3) development of computational models of stage-structured infection and immune responses to identify the types of costs that are most likely to lead to immune responses that differ across stages. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.