The Ecological Basis of an Emergent Behavioral Trait

Abstract

Organisms develop and evolve in complex and multi-faceted environments. While the development of the phenotype is generally considered to be due to processes internal to the organism, with the environment acting primarily as a source of selection, phenotypes are produced as a result of reciprocal interactions between internal organismal qualities and the environment. Thus, a phenotype encompasses all of the factors that contribute to its ontogeny, such as other individuals and microhabitat, with the consequence that the developmental system of one individual is often different from that of its parents. For this reason, individual development is subject to the vagaries of life experiences across the life cycle, yet despite this enormous variation in local experience, regularity at the population-level, such as population cycles, emerge. Broadly, how do interactions across scales influence evolution? In this dissertation, I investigated how interactions across local and population scales produced variation in behavioral strategies expressed by breeding birds to answer several key questions. First, given that the developmental system producing the phenotype of the parents often differs from that of the offspring, what is the impact of a mismatch between maternal and offspring environment on the trait expression of offspring? How can the incredibly variable experience of individuals produce specific patterns of offspring trait variation relative to environmental context? Why may population cycles emerge from variable individual experience? And lastly, what mechanisms within taxa may produce recurrent behavioral evolution across taxa? I investigated these questions using variation in the parental care strategies of western bluebirds (Sialia mexicana). My first chapter explored how a mismatch between maternal and offspring environment influenced the expression of parental care strategies in offspring. We found that when there was a mismatch between maternal and offspring experience in competition over resource availability, maternal influence on offspring aggression led to offspring pursuing a rare alternative behavioral strategy with lower fitness outcomes, but only when the environmental contexts across generations were not concordant. In this sense, behavioral variation emerged at the individual level when there was disconnect between local experience and conditions at the population level. While the evolution of adaptive maternal effects are thought to require specific, predictable cues to evolve, such specificity necessarily limits the breadth of environments in which maternally-induced traits function. Moreover, female experience is highly variable across ecological contexts, yet across females, maternal influence produces repeatable, specific offspring behavioral phenotypes. What processes allow for local complexity to be translated into specific outcomes? In my second chapter, I tested the hypothesis that the adaptive maternal effects did not evolve to track specific environmental cues, but instead used a general pathway (HPA stress response axis) that integrated maternal experience of multiple environmental factors. By combining long-term data spanning diverse environmental contexts with a large-scale field experiment, we showed that multiple environmental cues can alter maternal stress hormone levels (corticosterone), that variation in maternal corticosterone predicted offspring trait variation in aggression, and that expression of the maternal effect could not be explained by a single cue. Together, these data indicate that this adaptive maternal effect functions because it can accommodate multiple environmental stressors. Maternal stress pathways can respond to a wide variety of environmental stimuli, and thus this maternal effect can produce appropriate dispersal patterns in offspring, despite wide variation in the habitats that females encounter. Offspring behavioral phenotypes result from an interaction between both maternal and offspring environments, which may produce trait variation in many individuals at one time. For this reason, maternal effects are thought to be a potent regulator of population dynamics, because they may mediate feedbacks between offspring phenotype and environmental conditions. In my third chapter, I tested this idea by performing local manipulations of maternal experience across five replicate populations. I found that decreasing female experience of competition increased recruitment of sons. Lastly, in my fourth chapter, I explore the physiological mechanisms that may produce the recurrent emergence of cooperative breeding. Cooperative breeding has evolved across diverse avian taxa residing in very different environments, thus determining how local trait variation interacts with ecology to promote evolution of cooperative breeding strategies is an important question.