From mechanism to ecosystem: building bridges between ecoimmunology, psychoneuroimmunology and disease ecology.

Historically, the fields of ecoimmunology, psychoneuroimmunology and disease ecology have taken complementary yet disparate theoretical and experimental approaches, despite sharing critical common themes. Researchers in these areas have largely worked independently of one another to understand mechanistic immunological responses, organismal level immune performance, behavioral changes, and host and parasite/disease population dynamics, with few bridges across disciplines. Although efforts to strengthen and expand these bridges have been called for (and occasionally heeded) over the last decade, more integrative studies are only now beginning to emerge, with critical gaps remaining. Here, we briefly discuss the origins of these key fields, and their current state of integration, while highlighting several critical directions that we suggest will strengthen their connections into the future. Specifically, we highlight three key research areas that provide collaborative opportunities for integrative investigation across multiple levels of biological organization, from mechanisms to ecosystems: (1) parental effects of immunity, (2) microbiome and immune function and (3) sickness behaviors. By building new bridges among these fields, and strengthening existing ones, a truly integrative approach to understanding the role of host immunity on individual and community fitness is within our grasp.

The social environment alters neural responses to a lipopolysaccharide challenge.

Sick animals display drastic changes in their behavioral patterns, including decreased activity, decreased food and water intake, and decreased interest in social interactions. These behaviors, collectively called "sickness behaviors", can be socially modulated. For example, when provided with mating opportunities, males of several species show reduced sickness behaviors. While the behavior is known to change, how the social environment affects neural molecular responses to sickness is not known. Here, we used a species, the zebra finch, Taeniopygia guttata, where males have been shown to decrease sickness behaviors when presented with novel females. Using this paradigm, we obtained samples from three brain regions (the hypothalamus, the bed nucleus of the stria terminalis, and the nucleus taeniae) from lipopolysaccharide (LPS) or control treated males housed under four different social environments. Manipulation of the social environment rapidly changed the strength and co-expression patterns of the neural molecular responses to the immune challenge in all brain regions tested, therefore suggesting that the social environment plays a significant role in determining the neural responses to an infection. In particular, brains of males paired with a novel female showed muted immune responses to LPS, as well as altered synaptic signaling. Neural metabolic activity in response to the LPS challenge was also affected by the social environment. Our results provide new insights into the effects of the social environment on brain responses to an infection, thereby improving our understanding of how the social environment can affect health.

Neurotranscriptomic changes associated with chick-directed parental care in adult non-reproductive Japanese quail.

For many species, parental care critically affects offspring survival. But what drives animals to display parental behaviours towards young? In mammals, pregnancy-induced physiological transformations seem key in preparing the neural circuits that lead towards attraction (and reduced-aggression) to young. Beyond mammalian maternal behaviour, knowledge of the neural mechanisms that underlie young-directed parental care is severely lacking. We took advantage of a domesticated bird species, the Japanese quail, for which parental behaviour towards chicks can be induced in virgin non-reproductive adults through a sensitization procedure, a process that is not effective in all animals. We used the variation in parental responses to study neural transcriptomic changes associated with the sensitization procedure itself and with the outcome of the procedure (i.e., presence of parental behaviours). We found differences in gene expression in the hypothalamus and bed nucleus of the stria terminalis, but not the nucleus taeniae. Two genes identified are of particular interest. One is neurotensin, previously only demonstrated to be causally associated with maternal care in mammals. The other one is urocortin 3, causally demonstrated to affect young-directed neglect and aggression in mammals. Because our studies were conducted in animals that were reproductively quiescent, our results reflect core neural changes that may be associated with avian young-directed care independently of extensive hormonal stimulation. Our work opens new avenues of research into understanding the neural basis of parental care in non-placental species.