The transition from a sexual to a parental brain via nest building
Lead Research Organisation:
University of St Andrews
Department Name: Biology
Abstract
We propose that nest building, a widespread avian behaviour, offers a unique window to understand how species transition from a sexual to a parental brain. In most avian species, the sexual phase of reproduction is characterised by inter- and intra-sex behavioural interactions such as territoriality, courtship and mate guarding. This is followed by parental behaviours that ensure reproductive success. Some neuroendocrine changes that support sexual behaviour and parenthood are well characterised in birds. However, those underlying the rapid transition from a sexual to a parental brain are yet to be described, raising important fundamental questions regarding the variation observed both within and between species on this critical period of transition.
Bird reproductive activities are organised by the hypothalamic-pituitary-gonadal (HPG) axis. This finely tuned system orchestrates central and peripheral hormone release enabling breeding to commence only when environmental conditions are good enough for successful offspring rearing. In response to HPG axis stimulation, the gonads produce sex-steroid hormones, including testosterone and 17B-oestradiol, that act centrally to regulate reproductive behaviour. Bird embryos are exposed to environmental changes, such as daily temperature fluctuations or predation during development. To mitigate these risks, most birds build nests into which their eggs are laid and incubated, and the offspring reared.
We have previously established in zebra finches, Taeniopygia guttata, that circulating testosterone levels vary significantly towards the end of nest building, and that both sex-steroid sensitive and insensitive brain areas are active during this behaviour. Here we propose to establish where sex steroids act in the brain and the molecular and functional pathway(s) underlying key breeding stage transitions. Combining cutting-edge technologies, we will characterise the local variation(s) of sex steroids and their dedicated receptors in discrete brain areas during courtship, nest building and early incubation, and relate them to detailed behavioural analyses to better understand each of these behaviour/hormone relationships (Objective 1). We will also determine the main mechanisms through which sex steroids influence these behaviours using pharmacological manipulations (Objective 2). Using next generation sequencing and advanced bioinformatic analyses, we will determine which genes show expression changes in previously identified brain regions known to be sites of sex steroid sensitivity (Objective 3). Finally, in Objective 4 we will use neuronal tracing to characterise brain regions and neuronal networks that are strongly activated during nest building and are sex-steroid sensitive (Objective 4).
Thus, by performing the first comprehensive characterisation of the fine-scale variations in sex steroids and their receptors in the brain during rapid behavioural transitions, coupled with a detailed characterisation of the molecular and cellular networks they support, we will better understand how the brain supports the transition from sexual to parental reproductive phase in birds.
Bird reproductive activities are organised by the hypothalamic-pituitary-gonadal (HPG) axis. This finely tuned system orchestrates central and peripheral hormone release enabling breeding to commence only when environmental conditions are good enough for successful offspring rearing. In response to HPG axis stimulation, the gonads produce sex-steroid hormones, including testosterone and 17B-oestradiol, that act centrally to regulate reproductive behaviour. Bird embryos are exposed to environmental changes, such as daily temperature fluctuations or predation during development. To mitigate these risks, most birds build nests into which their eggs are laid and incubated, and the offspring reared.
We have previously established in zebra finches, Taeniopygia guttata, that circulating testosterone levels vary significantly towards the end of nest building, and that both sex-steroid sensitive and insensitive brain areas are active during this behaviour. Here we propose to establish where sex steroids act in the brain and the molecular and functional pathway(s) underlying key breeding stage transitions. Combining cutting-edge technologies, we will characterise the local variation(s) of sex steroids and their dedicated receptors in discrete brain areas during courtship, nest building and early incubation, and relate them to detailed behavioural analyses to better understand each of these behaviour/hormone relationships (Objective 1). We will also determine the main mechanisms through which sex steroids influence these behaviours using pharmacological manipulations (Objective 2). Using next generation sequencing and advanced bioinformatic analyses, we will determine which genes show expression changes in previously identified brain regions known to be sites of sex steroid sensitivity (Objective 3). Finally, in Objective 4 we will use neuronal tracing to characterise brain regions and neuronal networks that are strongly activated during nest building and are sex-steroid sensitive (Objective 4).
Thus, by performing the first comprehensive characterisation of the fine-scale variations in sex steroids and their receptors in the brain during rapid behavioural transitions, coupled with a detailed characterisation of the molecular and cellular networks they support, we will better understand how the brain supports the transition from sexual to parental reproductive phase in birds.
Technical Summary
We propose that nest building, a widespread avian behaviour, offers a unique opportunity to understand how species rapidly transition from sexual to parental behaviour and may provide insights into the observed individual variation in the timescale of the transition. We have previously established in male zebra finches, T. guttata, that circulating testosterone levels are high during courtship and nest building but drop rapidly shortly after the nest is built.
A fundamental outstanding question is, where in the brain, and through which pathway(s), sex steroids act to support sexual behaviours and the rapid transition into parental behaviours. We will first characterise local variations in sex steroids, cognate receptors, and metabolising enzymes by developing sex-steroid micro-LESA-LC-MS for the avian brain and coupling it with detailed histological and behavioural analyses. This will allow us to understand the behavioural neuroendocrine mechanisms responsible during courtship, nest building and early incubation (Objective 1). We will then determine the specific contribution to these transitions made by sex steroids using pharmacological approaches (Objective 2). Coupled together, these two objectives will highlight where and how specific sex steroids vary across early breeding phases and influence behaviour. Using Next Generation Sequencing, we will dissect the transcriptional and translational regulatory neural network changes across courtship to nest building (Objective 3). We previously established that both sex-steroid sensitive and insensitive brain areas are active during nest building; here we will use neuronal tracers to characterise the neural pathways supporting this behaviour (Objective 4).
Taken together, we will establish significant insight into the neurohormonal mechanisms supporting early breeding stages in birds and will shed light on how the brain supports the transition from a sexual to a parental phase during rapid reproductive events.
A fundamental outstanding question is, where in the brain, and through which pathway(s), sex steroids act to support sexual behaviours and the rapid transition into parental behaviours. We will first characterise local variations in sex steroids, cognate receptors, and metabolising enzymes by developing sex-steroid micro-LESA-LC-MS for the avian brain and coupling it with detailed histological and behavioural analyses. This will allow us to understand the behavioural neuroendocrine mechanisms responsible during courtship, nest building and early incubation (Objective 1). We will then determine the specific contribution to these transitions made by sex steroids using pharmacological approaches (Objective 2). Coupled together, these two objectives will highlight where and how specific sex steroids vary across early breeding phases and influence behaviour. Using Next Generation Sequencing, we will dissect the transcriptional and translational regulatory neural network changes across courtship to nest building (Objective 3). We previously established that both sex-steroid sensitive and insensitive brain areas are active during nest building; here we will use neuronal tracers to characterise the neural pathways supporting this behaviour (Objective 4).
Taken together, we will establish significant insight into the neurohormonal mechanisms supporting early breeding stages in birds and will shed light on how the brain supports the transition from a sexual to a parental phase during rapid reproductive events.