From Fur to Feathers: Mechanisms Regulating Reproductive Flexibility and Life History Trade-off Dynamics

Reproduction is a physiologically costly life history stage that varies widely in resource andbehavioral demands depending on the specific stage of courting, mating, and period of parental care. Seasonal shifts in environmental conditions influence animal energy budgets in ways which shape species’ life histories. Animals allocate energy and nutrients among a suite of competing physiological demands across short-, and long-term, timescales and the expression of specific traits or allocation strategy is tightly linked to the environment. Constraints on behavior and/or physiology have important implications for individual fitness and life history evolution, often leading to tradeoffs between processes supporting survival versus those supporting reproduction. In Chapter 1, I provide the first neuroanatomical description of RFRP (precursor peptide of gonadotropin-inhibitory hormone, GnIH) expression and localization in the brain of any bat using a widespread temperate species (Eptesicus fuscus, big brown bat) as a model. We show that RFRP transcripts occur in the hypothalamus, testes, and ovaries of big brown bats. Cellular RFRP immunoreactivity was observed across the hypothalamus, arcuate nucleus, and median eminence (ME), most similar to what is known in naked mole rats. RFRP fiber immunoreactivity was widespread as in other vertebrates. Putative interactions between RFRP-ir fibers and gonadotropinreleasing hormone cell bodies were observed in 16% of GnRH cells, suggesting potential for direct regulation of GnRH via RFRP signaling. This strengthens our fundamental knowledge of how the HPG axis may be regulated in bats and may now guide functional approaches to understanding how reproductive neurophysiology responds, or be well-adapted, to seasonal environmental cues and stressors. Animals face unpredictable challenges that require rapid, facultative physiological reactions to support survival but may compromise reproduction. Bats have a longstanding reputation for being highly sensitive to stressors, with sensitivity and resilience varying both within and among species. yet little is known about how stress affects the signaling that regulates reproductive physiology. Chapter 2 provides the first description of the molecular response of the hypothalamic-pituitary gonadal (HPG) axis of male big brown bats (E. fuscus) in response to short-term stress using a 2 standardized restraint manipulation. This acute stressor was sufficient to upregulate plasma corticosterone and resulted in a rapid decrease in circulating testosterone. While we did not find differences in the mRNA expression of key steroidogenic enzymes (StAR, aromatase, 5-alpha reductase), seminiferous tubule diameter was reduced in stressed bats coupled with a 5-fold increase in glucocorticoid receptor (GR) mRNA expression in the testes. These changes, in part, may be mediated by RFamide-related peptide (RFRP) because fewer immunoreactive cell bodies were detected in the brains of stressed bats compared to controls—suggesting a possible increase in secretion—and increased RFRP expression locally in the gonads. The rapid sensitivity of the bat testes to stress may be connected to deleterious impacts on tissue health and function as supported by significant transcriptional upregulation of key pro-apoptotic signaling molecules (Bax, cytochromec). Experiments like this broadly contribute to our understanding of the stronger ecological predictions regarding physiological responses of bats within the context of stress which may impact decisions surrounding animal handling and conservation approaches. Chapter 3 shifts from examining molecular mechanisms and neuroendocrinology regulating reproduction to a whole organism approach. Using a well-established captive colony of zebra finches, I characterize the behavioral and physiological conflicts between self-maintenance and reproductive investment and the factors that influence responses in line with energy limitation and/or trade-offs. Animals are faced with unpredictable challenges – such as pathogen exposure or infection – requiring quick physiological responses that support survival and may compromise resource allocation to reproduction. Stereotypical “sickness behaviors” may represent an energetic strategy that reduces investment in unnecessary activities to allocate resources toward – and support – the immune system. I use a framework of avian breeding stages to demonstrate the context-dependent behavioral conflict that may/may not be present across a species’ breeding period, and the importance of examining these conflicts through a holistic lens that takes species’ sociality and mating system into account as these variables directly affect routine individual energetic demands.

Advisor: Bentley, George E