Expression Patterns of Neuroligin-3 and Tyrosine Hydroxylase across the Brain in Mate Choice Contexts in Female Swordtails

Abstract

Choosing mates is a commonly shared behavior across many organisms, with important fitness consequences. Variations in female preferences can be due in part to differences in neural and cellular activity during mate selection. Initial studies have begun to identify putative brain regions involved in mate preference, yet the understanding of the neural processes regulating these behaviors is still nascent. In this study, we characterized the expression of a gene involved in synaptogenesis and plasticity (neuroligin-3) and one that codes for the rate-limiting enzyme in dopamine biosynthesis (tyrosine hydroxylase; TH1) in the female Xiphophorus nigrensis (northern swordtail) brain as related to mate preference behavior. We exposed females to a range of different mate choice contexts including two large courting males (LL), two small coercive males (SS), and a context that paired a large courting male with a small coercive male (LS). Neuroligin-3 expression in a mate preference context (LS) showed significant correlations with female preference in two telencephalic areas (Dm and Dl), a hypothalamic nucleus (HV), and two regions associated with sexual and social behavior (POA and Vv). We did not observe any context- or behavior-specific changes in tyrosine hydroxylase mRNA expression concomitant with female preference in any of the brain regions examined. Analysis of TH and neuroligin-3 expression across different brain regions showed that expression patterns varied with the male social environment only for neuroligin-3, where the density of correlated expression between brain regions was positively associated with mate choice contexts that involved a greater number of courting male phenotypes (LS and LL). This study identified regions showing presumed high levels of synaptic plasticity using neuroligin-3, implicating and supporting their roles in female mate preference, but we did not detect any relationship between tyrosine hydroxylase and mate preference with 30 min of stimulus presentation in X. nigrensis. These data suggest that information about potential mates is processed in select forebrain regions and the entire brain shows different degrees of correlated expression depending on the mate preference context.

Divergent neurogenomic responses shape social learning of both personality and mate preference

“…After all behavioral trials, we returned females to their respective treatment for an additional 2 months prior to tissue collection. We chose this time frame to minimize shortterm effects from mating preference trials, which have previously been studied in other systems and contexts (Bloch et al, 2018;Wong et al, 2012;Wong and Cummings, 2014), and focus our analysis instead on the effects of social exposure on baseline gene expression profiles.…”

“…In addition to examining transcriptome-wide data, we assessed differential expression between B-EXP and M-EXP females in key gene families previously shown to be implicated in social decisionmaking (O'Connell and Hofmann, 2012), mate choice (Cummings, 2015;Wong and Cummings, 2014;Wong et al, 2012;Bloch et al, 2018) and stress-related personality traits (Backström and Winberg, 2017;Thörnqvist et al, 2018). Interestingly, we found that M-EXP females were characterized by greater expression of several genes related to the signaling pathways of dopamine, serotonin, oxytocin and progesterone, as well as neuropeptide receptor-related GPCRs, while B-EXP females mostly showed upregulation of olfactory receptors and MHC-I-like genes (Fig.…”

Behavioral and brain- transcriptomic synchronization between the two opponents of a fighting pair of the fish Betta splendens

“…In recent years, an approach to map a specialized part of the brain by focusing on regions such as the hippocampus, which is involved in learning and memory [78,79], has been developed. A comparison of gene expression profiles among brain regions (e.g., telencephalon, diencephalon, cerebellum) in fish responding to intruders [70] has been attempted, and analyses of changes in the conserved 'social behavior network'-a collection of brain nuclei known to regulate social behaviors across vertebrates-based on detailed micro-dissected brain regions in cichlids [80], zebrafish [81], and swordtail fish [82] have been carried out. The limbic region, midbrain, and the cortical region are involved in a variety of motivations in mice [38,39,83].…”

Social Plasticity in the Fish Brain: Neuroscientific and Ethological Aspects

“…is not due to species differences per se, but that females are responding more to male reproductive tactics than species identity. Finally, in X. nigrensis, females exposed to two courting males show a high correlation in the expression of neuroligin-3 in regions that are associated with social decision making than females exposed to a courting and a coercive male, and little correlation is observed across these regions when females are exposed to two coercive males (Wong and Cummings, 2014), suggesting that interaction with courting phenotypes, more than coercive phenotypes, demand engagement of brain plasticity (Figure 3).…”