Localizing Brain Regions Associated with Female Mate Preference Behavior in a Swordtail

Abstract

Female mate choice behavior is a critical component of sexual selection, yet identifying the neural basis of this behavior is largely unresolved. Previous studies have implicated sensory processing and hypothalamic brain regions during female mate choice and there is a conserved network of brain regions (Social Behavior Network, SBN) that underlies sexual behaviors. However, we are only beginning to understand the role this network has in pre-copulatory female mate choice. Using in situ hybridization, we identify brain regions associated with mate preference in female Xiphophorus nigrensis, a swordtail species with a female choice mating system. We measure gene expression in 10 brain regions (linked to sexual behavior, reward, sensory integration or other processes) and find significant correlations between female preference behavior and gene expression in two telencephalic areas associated with reward, learning and multi-sensory processing (medial and lateral zones of the dorsal telencephalon) as well as an SBN region traditionally associated with sexual response (preoptic area). Network analysis shows that these brain regions may also be important in mate preference and that correlated patterns of neuroserpin expression between regions co-vary with differential compositions of the mate choice environment. Our results expand the emerging network for female preference from one that focused on sensory processing and midbrain sexual response centers to a more complex coordination involving forebrain areas that integrate primary sensory processing and reward.

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations

“…In this study we used expression of the immediate early gene egr-1 as a surrogate for neural excitation, an approach that has frequently been used to explore the reception of conspecific mating signals (Hoke et al, 2004;Sockman et al, 2005;Maney et al, 2006;Wong et al, 2012). It is important to note, however, that immediate early genes are themselves important regulators of further genomic action.…”

Looking for sexual selection in the female brain

“…While these results suggest that we have captured parts of the genomic response coordinating preference, they do not necessarily show that these specific genes are the fundamental cause of this behaviour or that they represent conserved behavioural genomic differences between species with contrasting mate preference systems. We are currently conducting further work to characterize this pathway in terms of neural circuitry [69], as well as how these genomic pathways are distinct from pathways associated with general social affiliation [70]. These studies have demonstrated that circulating oestradiol levels do not correlate with changes in female preference behaviour nor the expression levels of various preference candidate genes at the whole brain level [70] or in specific brain regions [69].…”

“…We are currently conducting further work to characterize this pathway in terms of neural circuitry [69], as well as how these genomic pathways are distinct from pathways associated with general social affiliation [70]. These studies have demonstrated that circulating oestradiol levels do not correlate with changes in female preference behaviour nor the expression levels of various preference candidate genes at the whole brain level [70] or in specific brain regions [69]. These results provide further demonstration of the power of the swordtail system to explore the behavioural genomics of mate preference dissociated from reproductive state and hormonal effects.…”

Testing synaptic plasticity in dynamic mate choice decisions: N -methyl d -aspartate receptor blockade disrupts female preference

“…Our previous research identified dynamic expression patterns associated with preference behaviour during mate choice conditions in X. nigrensis females, including genes associated with synaptic plasticity, such as neuroserpin, neuroligin-3 and N-methyl D-aspartate receptor (NMDAR) [6,7,8,10]. Synaptic plasticity processes within the brain mediate dynamic learning and memory, and a critical component of the glutamatergic signalling underlying this plasticity is NMDAR [11].…”