Causes and Consequences of Personality: Early Life Stress, Breeding Success, and Brain Structural Variation Across the Lifespan in a Passerine Bird

Abstract

Personality traits are behaviors that vary among individuals and are consistent in expression over the lifespan of an individual. They are at the forefront of an individual’s response to challenges and due to their consistency in expression, can have far-reaching impacts on fitness, survival, and individual experience of the world. Personality traits are ubiquitous, having been found in diverse taxa across the tree of life. Yet, we are still far from fully understanding the mechanisms behind their stability in expression and how population-level variation in these traits is maintained. What mechanisms promote variation in these traits within populations, and what is behind their stable expression across the lifespan? In this dissertation, I investigate mechanisms that might promote both the individual-level variation within a population necessary for personality, the consequences of this variation for breeding success, and the relationship between personality and brain structure variation across the lifespan, with a focus on the brain regions which most relevant for personality trait variation. Chapter 1 reviews our existing understanding of behavior across life and whether it plays a unique role in the evolutionary process in contrast to other phenotypic traits. I investigate the questions posed in Chapters 2, 3, and 4 using a captive colony of zebra finches (Taeniopygia guttata) as a study system. Zebra finches are an excellent model organism to investigate these questions. They breed readily in captivity and are a model organism for brain studies, so we have a detailed understanding of their brain structure and developmental timing. Furthermore, they are robust to MRI and tolerate anesthesia well. To investigate mechanisms that may promote the population-level maintenance of personality traits, I first assess the impact of personality traits on breeding success within our zebra finch colony. In my second chapter, I test how different types of personality traits may impact fitness in different ways. In particular, social personality traits may impact fitness through mediating interactions with others, while the fitness effects of non-social personality traits may vary more with external environmental conditions. We found that external social context is most important for social traits, such as aggression, while for non-social traits, like fearfulness, individual experience is the most important. Our results support the idea that variation in social and non-social personality traits is linked to fitness through distinct mechanisms. Next, I investigate the role of the developmental environment in generating variation in personality traits among individuals. Exposure to hormones such as glucocorticoids in ontogeny can alter developmental trajectories, as well as anxiety and fearfulness behavior in adulthood. However, the precise mechanisms by which these hormones impact behavior are unknown. One possibility is that exposure to elevated glucocorticoids may directly alter brain structural development by inhibiting growth. In Chapter 3, I manipulate maternal corticosterone (CORT) exposure and measure the effects of this treatment on changes to yolk steroid hormone concentrations, offspring personality and brain structure development through structural MRI. We found that CORT treated females produced eggs with higher glucocorticoid concentrations, and offspring were smaller than control at 15 days. Sons but not daughters showed higher fear responses. In sons, CORT treatment offspring also varied in limbic system brain regions associated with fear variation, with some areas proportionately larger than control and some smaller. This suggests that although CORT has an overall detrimental effect on growth, regions within the brain responsible for personality variation may functionally vary in response to CORT. Finally, understanding how the brain is capable of longitudinal change across the lifespan is important for characterizing the consistency of personality traits. In Chapter 1, we discuss the idea of dynamic versus static views of phenotype and how a static view dismisses the large changes to phenotypes that can occur over a lifespan, even in relatively more stable structures. In Chapter 4, I investigate how personality variation relates to aging-related decreases in brain volumes over time. To test these questions, I scanned the brains of focal individuals at two time points using structural magnetic resonance imaging (MRI), with the first scan at shortly after reaching one year of age, and the second at two and a half years (middle age). We found that brain volumes decreased between the time points of this study but this decrease was not uniform throughout the brain, with some regions decreasing in volume and others remaining stable. Most personality traits measured did not influence the rate of brain volume loss. However, activity level significantly increased volume loss in our birds. These results indicate that some brain regions in zebra finches are more sensitive to aging-related change than others, particularly some of the areas most important for personality variation. Furthermore, variation in some personality traits may be able to alter aging-related trajectories of volume loss.