Abstract
BackgroundThe brain plays a critical role in upstream regulation of processes central to mating effort, parental effort, and self-maintenance. For seasonally breeding animals, the brain is likely mediating trade-offs among these processes within a short breeding season, yet research thus far has only explored neurogenomic changes from non-breeding to breeding states or select pathways (e.g., steroids) in male and/or lab-reared animals. Here, we use RNA-seq to explore neural plasticity in three behaviorally relevant neural tissues (ventromedial telencephalon [VmT], hypothalamus [HYPO], and hindbrain [HB]), comparing free-living female tree swallows (Tachycineta bicolor) as they shift from territory establishment to incubation. We additionally highlight changes in aggression-related genes to explore the potential for a neurogenomic shift in the mechanisms regulating aggression, a critical behavior both in establishing and maintaining a territory and in defense of offspring.ResultsHB had few differentially expressed genes, but VmT and HYPO had hundreds. In particular, VmT had higher expression of genes related to neuroplasticity and processes beneficial for competition during territory establishment, but down-regulated immune processes. HYPO showed signs of high neuroplasticity during incubation, and a decreased potential for glucocorticoid signaling. Expression of aggression-related genes also shifted from steroidal to non-steroidal pathways across the breeding season.ConclusionsThese patterns suggest trade-offs between enhanced activity and immunity in the VmT and between stress responsiveness and parental care in the HYPO, along with a potential shift in the mechanisms regulating aggression. Collectively, these data highlight important gene regulatory pathways that may underlie behavioral plasticity in females.
Highlights
The brain plays a critical role in upstream regulation of processes central to mating effort, parental effort, and self-maintenance
We focused on three brain regions – the hypothalamus (HYPO), ventromedial telencephalon (VmT), and hindbrain (HB) – that have been previously implicated in both early spring competition and later parental care behaviors [29, 34,35,36]
The most significant up-regulated genes during territory establishment in the VmT included genes involved in brain function, while those up-regulated during incubation included several genes involved in metabolism, like inositol-3-phosphate synthase 1 (ISYNA1), fructosebisphosphate aldolase A (ALDOA), and fatty acid desaturase 1 (FADS1) (Fig. 2)
Summary
The brain plays a critical role in upstream regulation of processes central to mating effort, parental effort, and self-maintenance. Seasonal work on females has been limited due to the relative lack of research on early breeding season competition [19] and the misconception that females are too “complex” given their reproductive endocrinology [20] This complexity is precisely why it is important to understand how the female brain changes from territory establishment to parenting. While there is some work in wild birds that demonstrates a genomic link between steroid-related genes and early spring behaviors (e.g., competitive aggression [32, 33]), genomic profiles during early breeding stages are relatively unknown It remains to be tested what neurogenomic mechanisms track the transition from early breeding season competition to the steep parental demands that follow in a female experiencing a dynamic social environment
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