The mate choice brain: comparing gene profiles between female choice and male coercive poeciliids

Abstract

Genes that mediate mate preferences potentially play a key role in promoting and maintaining biological diversity. In this study, we compare mate preference behavior in two related poeciliid fishes with contrasting behavioral phenotypes and relate these behavioral differences to gene profiles in the brain. Results reveal that one poeciliid fish, the Northern swordtail, exhibits robust mate preference as compared to the Western mosquitofish, which utilizes a coercive mating system. Female swordtails display no significant difference in association time between male-and female-exposure trials, whereas female mosquitofish spend significantly less time associating with males relative to females. Furthermore, the preference strength for large males is significantly lower in female mosquitofish relative to swordtails. We then examine expression of three candidate genes previously shown to be associated with mate preference behavior in female swordtails and linked to neural plasticity in other vertebrates: neuroserpin (NS), neuroligin-3 (NLG-3) and N-methyl-D-aspartate receptor (NMDA-R). Whole brain gene expression patterns reveal that two genes (NS and NLG-3) are positively associated with mate preference behavior in female swordtails, a pattern opposing that of the mosquitofish. In mosquitofish females, these genes are downregulated when females express biases toward males yet are elevated in association with total motor activity patterns under asocial conditions, suggesting that the presence of males in mosquitofish species may inhibit expression of these genes. Both gene expression and female behavioral responses to males exhibit opposing patterns between these species, suggesting that this genetic pathway may potentially act as a substrate for the evolution of mate preference behavior.

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

“…In the current experiment, we predicted that disrupted mate preference responses would be reflected in gene modules linked to dynamic preference behaviours if blocked glutamatergic signalling altered normal female responses to males. We measured expression for 11 genes previously associated with social behaviours in X. nigrensis females [6][7][8], including five synaptic-plasticitylinked genes associated with female preference (neuroserpin, neuroligin-3, NMDA-receptor, tPA and stathmin-2), four associated with female receptivity or socio-sexual behaviours (b-1 adrenergic receptor, a-1 adrenergic receptor, tyrosine hydroxylase and brain aromatase) and two associated with general social and reproductive behaviours in teleosts (vasotocin and isotocin). Preference/receptivity markers (including genes linked with synaptic plasticity) were associated with controls.…”

“…See the electronic supplementary material for detailed gene inclusion and expression assay parameters. Gene expression levels were normalized by deriving the residuals from a linear regression of the measured gene concentration by input cDNA concentration (as in [7,8] In LS-exposed females, total activity levels were unchanged by treatment (figure 1b), but there was a significant shift in the proportion of social to neutral behaviours in MK-801 females (figure 1c; pre versus post: MK-801: p ¼ 0.02; control: p ¼ 0.28; electronic supplementary material, table S1). By contrast, the ratio of social to neutral behaviours was not altered following MK-801 treatment in FF females (electronic supplementary material, figure S3) although overall activity did increase (MK-801: p ¼ 0.02; control: p ¼ 0.33), driven by increased neutral behaviours (MK-801: p ¼ 0.01; control: p ¼ 0.19).…”

“…While variation in female responses towards different male phenotypes can arise from numerous factors [1], increasing evidence indicates that the behavioural plasticity associated with vertebrate mate choice also involves learning [2]. For example, several poeciliids, including Xiphophorus nigrensis, show age-dependent changes in female preference functions [3][4][5] and express synaptic-plasticity-associated molecular markers during mate choice events [6][7][8].…”

“…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].…”

“…NMDAR antagonism disrupts multiple aspects of social learning and emotional processing [14 -18], therefore we included genes linked to both preference behaviours (e.g. neuroserpin, neuroligin-3, NMDAR [6][7][8]) and general sociality (isotocin and vasotocin-fish homologues of oxytocin and vasopressin [19 -21]) in fish to characterize the effects of disrupted social cognition on gene modules associated with these two critical aspects of mate choice behaviour.…”