PhD: Behavioral, Physiological, and Transcriptomic Variation Among Colonies of Pogonomyrmex barbatus

Social insect colony behavior arises within a specific ecological context from patterns of interactions of nestmates with each other. The neurophysiological basis of behavior in the social insects has primarily been studied in the context of behavioral differences among nestmates, for example between nursing and foraging workers. Many conserved pathways that regulate behavior in other animals, such as the neurohormonal and biogenic amine neurotransmitter signaling pathways, are also involved in generating behavioral variation among social insect nestmates. Less is known from a molecular perspective about how worker neurophysiological variation is associated with colony-level, collective, behaviors. In this thesis, I consider how physiological differences among colonies of the red harvester ant (Pogonomyrmex barbatus) are associated with colony behavioral differences, and with the evolution of collective behavior. Chapter 1 uses transcriptomic profiling of forager brains from P. barbatus colonies to explore differences in gene expression between groups of colonies that vary in how they regulate foraging in dry conditions. Forager brains of different colonies significantly varied in brain biogenic amine titers, as well as in the expression of multiple neurophysiological signaling pathways involved in regulating foraging in social and solitary insect species. Pharmacological experiments demonstrated that increases in forager brain dopamine titer resulted in increases in foraging activity, whereas decreases in brain dopamine decreased foraging activity. Chapter 2 investigates the relationship between colony foraging behavior, colony reproductive success, and forager desiccation physiology. Foragers from colonies that reduced foraging activity in dry conditions lose water and motor coordination more rapidly than foragers from colonies that did not reduce foraging in dry conditions. Manipulative experiments in the field show that hydrated foragers go on significantly more foraging trips than their unhydrated nestmates, and that this effect increases in strength as conditions get drier. Chapter 3 uses RNA-seq on single forager brains to investigate how variation in gene expression variation within and among colonies is associated with colony traits and with the degree of protein coding sequence constraint over evolutionary time. Hundreds of genes had expression and coexpression patterns correlated with colony traits. Gene coexpression modules were significantly differentially utilized among colonies, and these modules were enriched in neurophysiologically-relevant functions related to the regulation of biogenic metabolism and signaling. Loci that are more central to coexpression networks tend to be better correlated with colony traits, and are evolving under increased coding sequencing constraint relative to less central loci. Chapter 4 uses pharmacological experiments on individually-marked foragers to characterize how heterogeneity among nestmates in foraging activity was related to the effect of hydration and dopamine treatment on increasing overall foraging trips. The overall stimulatory effect of hydration and dopamine treatment was not due to a small subset of ants. The relationship between humidity and foraging activity was more variable within a day and between colonies, than between different treatment groups. Natural selection shapes patterns of behavioral variation among ant colonies via the differential reproductive success of colonies with different phenotypes. Colony behavioral variation arises from a complex nexus of both heritable and non-heritable factors. All molecular factors exert their influence on colony behavior only to the extent that they modulate worker physiology to alter how workers respond to different types of interactions. This thesis begins to characterize the neurophysiological basis of variation among red harvester ant colonies in foraging behavior.

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