Sex differences in cognitive performance and style across domains in mosquitofish (Gambusia affinis).

Given that the sexes often differ in their ecological and sexual selection pressures, sex differences in cognitive properties are likely. While research on sexually dimorphic cognition often focuses on performance, it commonly overlooks how sexes diverge across cognitive domains and in behaviors exhibited during a cognitive task (cognitive style). We tested male and female western mosquitofish (Gambusia affinis) in three cognitive tasks: associative learning (numerical discrimination), cognitive flexibility (detour task), and spatio-temporal learning (shuttlebox). We characterized statistical relationships between cognitive performances and cognitive style during the associative learning task with measures of anxiety, boldness, exploration, reaction time, and activity. We found sex differences in performance, cognitive style, and the relationships between cognitive domains. Females outperformed males in the spatio-temporal learning task, while the sexes performed equally in associate learning and cognitive flexibility assays. Females (but not males) exhibited a 'fast-exploratory' cognitive style during associative learning trials. Meanwhile, only males showed a significant positive relationship between domains (associative learning and cognitive flexibility). We propose that these sexually dimorphic cognitive traits result from strong sexual conflict in this taxon; and emphasize the need to explore suites of sex-specific cognitive traits and broader comparative work examining sexual selection and cognition.

Isotocin increases female avoidance of males in a coercive mating system: Assessing the social salience hypothesis of oxytocin in a fish species.

The nonapeptide oxytocin (and its fish homolog isotocin (IT)) is an evolutionarily-conserved hormone associated with social behaviors across most vertebrate taxa. Oxytocin has traditionally been regarded as a prosocial hormone, but studies on social cognition in mammalian models suggest it may play a more nuanced role in modulating social discrimination based on social salience and stimulus valence. Here we test IT and its role in regulating female social decision-making and anxiety behaviors in a live-bearing fish with a male coercive mating system. Gambusia affinis males engage in a forced mating strategy, with frequent harassment and attempted copulatory thrusts directed towards unwilling females. Exogenous IT produced anxiolytic responses in female G. affinis that altered exploration (time in center of tank) but not time in dark vs. light regions of the tank. Exogenous IT also produced context-specific changes in social tendency: IT-treated G. affinis females spent less time associating with males while association time with conspecific females was not altered. Further, while overall activity levels were not changed by IT treatment, the amount of social behaviors IT-treated females directed towards males, but not females, was reduced. Our results support the social salience hypothesis of oxytocin action in a teleost and suggest that oxytocin's critical input into social cognitive processing is conserved across vertebrate taxa.

Differential sensitivity to estrogen-induced opsin expression in two poeciliid freshwater fish species.

The sensory system shapes an individual's perception of the world, including social interactions with conspecifics, habitat selection, predator detection, and foraging behavior. Sensory signaling can be modulated by steroid hormones, making these processes particularly vulnerable to environmental perturbations. Here we examine the influence of exogenous estrogen manipulation on the visual physiology of female western mosquitofish (Gambusia affinis) and sailfin mollies (Poecilia latipinna), two poeciliid species that inhabit freshwater environments across the southern United States. We conducted two experiments to address this aim. First, we exposed females from both species to a one-week dose response experiment with three treatments of waterborne ß-estradiol. Next, we conducted a one-week estrogen manipulation experiment with a waterborne estrogen (ß-Estradiol), a selective estrogen receptor modulator (tamoxifen), or combination estrogen and tamoxifen treatment. We used quantitative PCR (qPCR) to examine the expression of cone opsins (SWS1, SWS2b, SWS2a, Rh2, LWS), rhodopsin (Rh1), and steroid receptor genes (ARα, ARß, ERα, ERß2, GPER) in the eyes of individual females from each species. Results from the dose response experiment revealed estradiol-sensitivity in opsin (SWS2a, Rh2, Rh1) and androgen receptor (ARα, ARß) gene expression in mosquitofish females, but not sailfins. Meanwhile, our estrogen receptor modulation experiments revealed estrogen sensitivity in LWS opsin expression in both species, along with sensitivity in SWS1, SWS2b, and Rh2 opsins in mosquitofish. Comparisons of control females across experiments reveal species-level differences in opsin expression, with mosquitofish retinas dominated by short-wavelength sensitive opsins (SWS2b) and sailfins retinas dominated by medium- and long-wavelength sensitive opsins (Rh2 and LWS). Our research suggests that variation in exogenous levels of sex hormones within freshwater environments can modify the visual physiology of fishes in a species-specific manner.

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

Social behaviours such as mate choice require context-specific responses, often with evolutionary consequences. Increasing evidence indicates that the behavioural plasticity associated with mate choice involves learning. For example, poeciliids show age-dependent changes in female preference functions and express synaptic-plasticity-associated molecular markers during mate choice. Here, we test whether social cognition is necessary for female preference behaviour by blocking the central player in synaptic plasticity, NMDAR (N-methyl d-aspartate receptor), in a poeciliid fish, Xiphophorus nigrensis. After subchronic exposure to NMDAR antagonist MK-801, female preference behaviours towards males were dramatically reduced. Overall activity levels were unaffected, but there was a directional shift from 'social' behaviours towards neutral activity. Multivariate gene expression patterns significantly discriminated between females with normal versus disrupted plasticity processes and correlated with preference behaviours-not general activity. Furthermore, molecular patterns support a distinction between 'preference' (e.g. neuroserpin, neuroligin-3, NMDAR) and 'sociality' (isotocin and vasotocin) gene clusters, highlighting a possible conservation between NMDAR disruption and nonapeptides in modulating behaviour. Our results suggest that mate preference may involve greater social memory processing than overall sociality, and that poeciliid preference functions integrate synaptic-plasticity-oriented 'preference' pathways with overall sociality to invoke dynamic, context-specific responses towards favoured males and away from unfavoured males.

Estradiol, reproductive cycle and preference behavior in a northern swordtail.

Estrogen is associated with female sexual behaviors, particularly receptive behaviors during the reproductive cycle. Less is known about the relationship between estrogen and female preference behaviors that may precede receptivity and copulation. Separating the mechanisms underlying preference from receptivity is often confounded by the tightly coupled cycle- or estrogen-dependent expression of female sexual behaviors. Here we utilize a live-bearing poeciliid (Xiphophorus nigrensis), a model species for studying the evolution of female mate choice that can store sperm over multiple brood cycles. We assayed estradiol along with preference, receptivity and locomotor behaviors in gestating females and then re-tested these females on days 1, 7, 14, 21, and 28 post-parturition. With a posteriori reproductive cycle assessment, we asked whether reproductive state predicts differences in (i) estradiol levels, and (ii) behaviors (preference, receptivity, and general locomotor activity). We then examined if estradiol levels (independent of reproductive state) explain any variation in these behaviors. We found that endogenous estradiol levels vary across the reproductive cycle: gestating females had lower estradiol levels than those undergoing vitellogenesis/fertilization. In contrast, receptivity and preference behaviors did not vary over the reproductive cycle. Estradiol levels did not predict variation in receptive behavior, but were associated with increased locomotion. While individual female preference behaviors were consistent across the reproductive cycle, there was a small negative relationship between estradiol and preference behaviors explaining between 3% and 10% of the inter-female variation in preference behavior. Our data indicate X. nigrensis females may exhibit a facultatively dissociated reproductive system.

Overlooking the obvious: a meta-analytic comparison of digit symbol coding tasks and other cognitive measures in schizophrenia.

CONTEXT: In focusing on potentially localizable cognitive impairments, the schizophrenia meta-analytic literature has overlooked the largest single impairment: on digit symbol coding tasks. OBJECTIVE: To compare the magnitude of the schizophrenia impairment on coding tasks with impairments on other traditional neuropsychological instruments. DATA SOURCES: MEDLINE and PsycINFO electronic databases and reference lists from identified articles. STUDY SELECTION: English-language studies from 1990 to present, comparing performance of patients with schizophrenia and healthy controls on coding tasks and cognitive measures representing at least 2 other cognitive domains. Of 182 studies identified, 40 met all criteria for inclusion in the meta-analysis. DATA EXTRACTION: Means, standard deviations, and sample sizes were extracted for digit symbol coding and 36 other cognitive variables. In addition, we recorded potential clinical moderator variables, including chronicity/severity, medication status, age, and education, and potential study design moderators, including coding task variant, matching, and study publication date. DATA SYNTHESIS: Main analyses synthesized data from 37 studies comprising 1961 patients with schizophrenia and 1444 comparison subjects. Combination of mean effect sizes across studies by means of a random effects model yielded a weighted mean effect for digit symbol coding of g = -1.57 (95% confidence interval, -1.66 to -1.48). This effect compared with a grand mean effect of g = -0.98 and was significantly larger than effects for widely used measures of episodic memory, executive functioning, and working memory. Moderator variable analyses indicated that clinical and study design differences between studies had little effect on the coding task effect. Comparison with previous meta-analyses suggested that current results were representative of the broader literature. Subsidiary analysis of data from relatives of patients with schizophrenia also suggested prominent coding task impairments in this group. CONCLUSION: The 5-minute digit symbol coding task, reliable and easy to administer, taps an information processing inefficiency that is a central feature of the cognitive deficit in schizophrenia and deserves systematic investigation.

Localizing brain regions associated with female mate preference behavior in a swordtail.

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.

Identifying context-specific gene profiles of social, reproductive, and mate preference behavior in a fish species with female mate choice.

Sensory and social inputs interact with underlying gene suites to coordinate social behavior. Here we use a naturally complex system in sexual selection studies, the swordtail, to explore how genes associated with mate preference, receptivity, and social affiliation interact in the female brain under specific social conditions. We focused on 11 genes associated with mate preference in this species (neuroserpin, neuroligin-3, NMDA receptor, tPA, stathmin-2, ß-1 adrenergic receptor) or with female sociosexual behaviors in other taxa (vasotocin, isotocin, brain aromatase, α-1 adrenergic receptor, tyrosine hydroxylase). We exposed females to four social conditions, including pairings of differing mate choice complexity (large males, large/small males, small males), and a social control (two females). Female mate preference differed significantly by context. Multiple discriminant analysis (MDA) of behaviors revealed a primary axis (explaining 50.2% between-group variance) highlighting differences between groups eliciting high preference behaviors (LL, LS) vs. other contexts, and a secondary axis capturing general measures distinguishing a non-favored group (SS) from other groups. Gene expression MDA revealed a major axis (68.4% between-group variance) that distinguished amongst differential male pairings and was driven by suites of "preference and receptivity genes"; whereas a second axis, distinguishing high affiliation groups (large males, females) from low (small males), was characterized by traditional affiliative-associated genes (isotocin, vasotocin). We found context-specific correlations between behavior and gene MDA, suggesting gene suites covary with behaviors in a socially relevant context. Distinct associations between "affiliative" and "preference" axes suggest mate preference may be mediated by distinct clusters from those of social affiliation. Our results highlight the need to incorporate natural complexity of mating systems into behavioral genomics.