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

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... The visual pigment located in the photoreceptor outer segment is responsible for deciphering light information and it comprises a light-absorbing protein (visual opsin) and a vitamin A-derived chromophore. Visual opsins are membrane-bound but exactly how many cone opsins it has remains uncertain [32]. Moreover, previous studies indicate that the western mosquitofish may display ontogenetic changes in cone opsin expression profiles because it exhibits an ontogenetic dietary shift, colors are critical to it in the mating choice of both sexes, and sex steroid estrogen influences its cone opsin expression profiles [32][33][34][35][36]. ...
... Visual opsins are membrane-bound but exactly how many cone opsins it has remains uncertain [32]. Moreover, previous studies indicate that the western mosquitofish may display ontogenetic changes in cone opsin expression profiles because it exhibits an ontogenetic dietary shift, colors are critical to it in the mating choice of both sexes, and sex steroid estrogen influences its cone opsin expression profiles [32][33][34][35][36]. ...
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To convert external light into internal neural signal, vertebrates rely on a special group of proteins, the visual opsins. Four of the five types of visual opsins-short-wavelength sensitive 1 (Sws1), short-wavelength sensitive 2 (Sws2), medium-wavelength sensitive (Rh2), and long-wavelength sensitive (Lws)-are expressed in cone cells for scotopic vision, with the fifth, rhodopsin (Rh1), being expressed in rod cells for photopic vision. Fish often display differing ontogenetic cone opsin expression profiles, which may be related to dietary and/or habitat ontogenetic shift. The western mosquitofish (Gambusia affinis) is an aggressive invader that has successfully colonized every continent except Antarctica. The strong inva-siveness of this species may be linked to its visual acuity since it can inhabit turbid waters better than other fishes. By genome screening and transcriptome analysis, we identify seven cone opsin genes in the western mosquitofish, including one sws1, two sws2, one rh2, and three lws. The predicted maximal absorbance wavelength (λ max) values of the respective proteins are 353 nm for Sws1, 449 nm for Sws2a, 408 nm for Sws2b, 516 nm for Rh2-1, 571 nm for Lws-1, and 519 nm for Lws-3. Retention of an intron in the lws-r transcript likely renders this visual opsin gene non-functional. Our real-time quantitative PCR demonstrates that adult male and female western mosquitofish do not differ in their cone opsin expression profiles, but we do reveal an ontogenetic shift in cone opsin expression. Compared to adults, larvae express proportionally more sws1 and less lws-1, suggesting that the western mosquitofish is more sensitive to shorter wavelengths in the larval stage, but becomes more sensitive to longer wavelengths in adulthood.
... For example, aromatase has been found in the goldfish (Carassius auratus) retina, including in the inner nuclear layer Callard 1993, 1997). Additionally, the gene expression of several opsins in mosquitofish and sailfin molly females increases with increased estradiol exposure (Friesen et al. 2017b). Estrogen receptors in retinas have been found in a variety of species, including humans, bovines, rats, and fish (Begay et al. 1994;Kobayashi et al. 1998;Ogueta et al. 1999;Tchoudakova et al. 1999;Mangiamele et al. 2017). ...
... Relevant to vision, such receptors have been found in the retinas of humans (Ogueta et al. 1999). In fish retina their expression can be reproductively modulated (Tchoudakova et al. 1999;Friesen et al. 2017b;Butler et al. 2019). Estrogens can also have rapid, nongenomic effects 3 Comparison of ERG b-wave thresholds for the three treatment groups. ...
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Although mate searching behavior in female túngara frogs (Physalaemus pustulosus) is nocturnal and largely mediated by acoustic cues, male signaling includes visual cues produced by the vocal sac. To compensate for these low light conditions, visual sensitivity in females is modulated when they are in a reproductive state, as retinal thresholds are decreased. This study tested whether estradiol (E2) plays a role in this modulation. Female túngara frogs were injected with either human chorionic gonadotropin (hCG) or a combination of hCG and fadrozole. hCG induces a reproductive state and increases retinal sensitivity, while fadrozole is an aromatase inhibitor that blocks hCG-induced E2 synthesis. In an analysis of scotopic electroretinograms (ERGs), hCG treatment lowered the threshold for eliciting a b-wave response, whereas the addition of fadrozole abolished this effect, matching thresholds in non-reproductive saline-injected controls. This suggests that blocking E2 synthesis blocked the hCG-mediated reproductive modulation of retinal sensitivity. By implicating E2 in control of retinal sensitivity, our data add to growing evidence that the targets of gonadal steroid feedback loops include sensory receptor organs, where stimulus sensitivity may be modulated, rather than more central brain nuclei, where modulation may affect mechanisms involved in motivation.
... That study notwithstanding, compelling evidence for this phenomenon in other systems is largely indirect or lacking measures of sensitivity change in the sensory organ itself. For example, histological approaches have revealed steroid hormone receptors in the retinas of humans (Ogueta et al., 1999), goldfish (Tchoudakova et al., 1999), western mosquitofish, sailfin mollies (Friesen et al., 2017), and three-spined sticklebacks (Hoffmann et al., 2012). With respect to behavior, female and male three-spined sticklebacks show increased spectral sensitivity (as measured by optomotor response) to red light (which is characteristic of courting male coloration) during the breeding season (Cronly-Dillon and Sharma, 1968;Boulcott and Braithwaite, 2007). ...
... Studies have also demonstrated a neuroprotective effect of estrogen on the human retina and optic nerve (reviewed in Nuzzi et al., 2019). Aromatase (Gelinas and Callard, 1993) and estrogen receptor β (Tchoudakova et al., 1999) are both present in the retina of the goldfish, while a study of female western mosquitofish and sailfin mollies demonstrated various, speciesspecific effects of estrogen treatment on opsin and androgen receptor gene expression in the retina (Friesen et al., 2017). Androgen receptor β is present in eyes of both male and female three-spined sticklebacks (Gasterosteus aculeatus) (Hoffmann et al., 2012). ...
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Visual cues are often a vital part of animal communication and courtship. While a plethora of studies have focused on the role that hormones play in acoustic communication of anurans, relatively few have explored hormonal modulation of vision in these animals. Much of what we do know comes from behavioral studies, which show that a frog’s hormonal state can significantly affect both its visual behavior and mating decisions. However, to fully understand how frogs use visual cues to make these mating decisions, we must first understand how their visual system processes these cues, and how hormones affect these processes. To do this, we performed electroretinograms (ERGs) to measure retinal sensitivity of túngara frogs (Physalaemus pustulosus), a neotropical species whose mating behavior includes previously described visual cues. To determine the effect of hormonal state on visual sensitivity, ERGs were recorded under scotopic and photopic conditions in frogs that were either non-reproductive or hormone-treated with human chorionic gonadotropin (hCG) prior to testing. Additionally, measurements of optical anatomy determined how túngara frog eye and retina morphology related to physiological sensitivity. As expected, we found that both sexes display higher visual sensitivity under scotopic conditions compared to photopic conditions. However, hormone injections significantly increased retinal sensitivity of females under scotopic conditions. These results support the hypothesis that hormonal modulation of neural mechanisms, such as those mediating visually guided reproductive behavior in this species, include modulation of the receptor organ: the retina. Thus, our data serve as a starting point for elucidating the mechanism of hormonal modulation of visual sensitivity.
... glaucoma) (Vajaranant et al., 2010;Zhou et al., 2007). Estrogens may even be produced in the eye (Cascio et al., 2007), androgens were shown to affect visual sensitivity in male fishes (Shao et al., 2014;Yue et al., 2018), and exogenous estrogens influence opsin expression in the eye of mosquito fish (Friesen et al., 2017). Together, these data suggest that sex steroids play a neuromodulatory role in vision across taxa. ...
... Further, females had an ovulation-dependent increase in most of these receptors, indicating that this plasticity is dependent on endogenous hormonal state. Mosquitofish exposed to waterborne estrogen had altered levels of androgen receptors and the long-wavelength sensitive opsin in the eye, indicating that even exogenous hormones, in addition to endogenous ones, can alter expression of reproductive neuromodulatory receptors and other components of the visual system (Friesen et al., 2017). Our study is consistent with the hypothesis that reproductive-and hormonal-state modulation of vision at the level of the retina is conserved across vertebrates. ...
Article
Visual communication is used widely across the animal kingdom to convey crucial information about an animals' identity, reproductive status, and sex. Although it is well-demonstrated that auditory and olfactory sensitivity can change with reproductive state, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice behaviors in many species are largely dependent on visual signals. Here, we tested for reproductive state-dependent plasticity in the eye of the cichlid fish Astatotilapia burtoni using behavioral, gene expression, neural activation, and electrophysiology techniques. Males court ovulated females more intensely than gravid females, and ovulated females were more responsive to male courtship behaviors than gravid females. Using electroretinography to measure visual sensitivity in dark-adapted fish, we revealed that gravid, reproductively-ready females have increased visual sensitivity at wavelengths associated with male courtship coloration compared to non-gravid females. After ovulation was hormonally induced, female's spectral sensitivity further increased compared to pre-injection measurements. This increased sensitivity after hormone injection was absent in non-gravid females and in males, suggesting an ovulation-triggered increase in visual sensitivity. Ovulated females had higher mRNA expression levels of reproductive neuromodulatory receptors (sex-steroids; gonadotropins) in the eye than nonovulated females, whereas males had similar expression levels independent of reproductive/social state. In addition, female mate choice-like behaviors positively correlated with expression of gonadotropin system receptors in the eye. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.
... However, considering that this effect was not observed upon prolactin administration (Fig. 3, b and d), we suggest the prolactin independent changes in the expression of these opsins. Expression of RH2 and LWS during freshwater adaptation could be affected by estrogens, as these hormones were demonstrated to stim ulate expression of the RH2 and LWS genes in the retina of mosquitofish G. affinis [11]. Unlike in female stickle backs, expression of the RH2 and LWS genes in the retina of male sticklebacks did not change during the freshwater adaptation, and similarly to females, was not affected by prolactin administration (Fig. 6). ...
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Color vision sensitivity is crucial for fish adaptation during migration and reproduction. Prolactin and prolactin-like hormone are important regulators in both these processes. We hypothesized that prolactin influences the color vision sensitivity during freshwater migrations in fish. We studied the effects of prolactin and freshwater adaptation during the spawning period on the expression of opsin genes (SWS1, SWS2, RH2, LWS) in the retina of female and male three-spined sticklebacks Gasterosteus aculeatus L. Expression of the prolactin gene increased in the brain of females, but not males, while expression of the prolactin-like hormone decreased in the brain of both male and female sticklebacks during freshwater adaptation. Expression of the SWS2 gene decreased in the retina of females and males during freshwater adaptation and after prolactin administration. Expression of the SWS1 gene decreased in the retina of male sticklebacks after prolactin administration, but not during freshwater adaptation. Expression of the RH2 and LWS genes did not depend on prolactin administration in male and female sticklebacks. We conclude that expression of some opsin genes in the retina of sticklebacks is regulated by prolactin and depends on sex and freshwater adaptation. This expands our knowledge of the adaptive effects of prolactin on fish during freshwater migrations.
... Several studies have demonstrated that naturally occurring estrogens and synthetic analogs are effective neuroprotectants in retinal diseases, including age-related macular degeneration and diabetic retinopathy (Kumar et al., 2008). Similarly, the expression of rhodopsin is dose-dependent with the treatment of waterborne β-estradiol in mosquitofish females, indicating that estrogens might influence the visual perception based on their modulation of sensory systems (Friesen et al., 2017). However, the interaction between phototransduction and estrogen signaling pathways needs further investigation. ...
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Previously, we reported the myelin regulatory factor ( MYRF ) as a candidate gene for nanophthalmos. We have also produced Myrf knockdown ( Myrf +/− ) mouse strain to investigate the cellular and molecular phenotypes of reduced MYRF expression in the retina. Myrf +/− mouse strain was generated using the CRISPR/Cas9 system. Optomotor response system, electroretinogram (ERG), spectral-domain optical coherence tomography (SD-OCT), histology, and immunohistochemistry were performed to evaluate retinal spatial vision, electrophysiological function, retinal thickness, and pathological changes in cone or rod photoreceptors, respectively. RNA sequencing (RNA-seq) was performed to investigate the underlying molecular mechanism linking Myrf deficiency with photoreceptor defects. The genotype and phenotype of CRISPR/Cas9-induced Myrf +/− mice and their offspring were comprehensively investigated. Photoreceptor defects were detected in the retinas of Myrf +/− mice. Visual acuity and ERG responses were decreased in Myrf +/− mice compared with the control mice ( Myrf +/+ ). The loss of cone and rod neurons was proportional to the decreased outer nuclear layer (ONL) thickness. Moreover, RNA-seq revealed that phototransduction and estrogen signaling pathways played important roles in the Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis. Myrf +/− mouse strain provides a good model to investigate the function of the MYRF gene. Photoreceptor defects with impaired functions of spatial vision and retinal electrophysiology indicate an important role played by MYRF in retinal development. Alterations in phototransduction and estrogen signaling pathways play important roles in linking Myrf deficiency with retinal photoreceptor defects.
... Expression levels of SWS2 in female birds was correlated not only with habitat metrics, but also with an index of sexual selection (degree of plumage dichromatism), suggesting that the female visual system may co-evolve with male coloration patterns (Bloch, 2015). Hormonal modulation can also affect expression levels: a study of females of two poeciliid fish documented species-specific effects of sex steroids on opsin expression (Friesen et al., 2017). ...
Article
Sensory receptors enable animals to perceive their external world, and functional properties of receptors evolve to detect the specific cues relevant for an organism's survival. Changes in sensory receptor function or tuning can directly impact an organism's behavior. Functional tests of receptors from multiple species and the generation of chimeric receptors between orthologs with different properties allow for the dissection of the molecular basis of receptor function and identification of the key residues that impart functional changes in different species. Knowledge of these functionally important sites facilitates investigation into questions regarding the role of epistasis and the extent of convergence, as well as the timing of sensory shifts relative to other phenotypic changes. However, as receptors can also play roles in non-sensory tissues, and receptor responses can be modulated by numerous other factors including varying expression levels, alternative splicing, and morphological features of the sensory cell, behavioral validation can be instrumental in confirming that responses observed in heterologous systems play a sensory role. Comparative genomic approaches and expression profiling of sensory cells can identify other proteins under relaxed or positive selection, shed light on cell-type specific modifications that may affect receptor function and provide insight into the correlated evolution of complex suites of traits. Here we review the evolutionary history and diversity of functional responses of the major classes of sensory receptors in vertebrates, including opsins, chemosensory receptors, and ion channels involved in temperature-sensing, mechanosensation and electroreception.
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Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared to non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared to mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.
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Background The visual system is important for animals for mate choice, food acquisition, and predator avoidance. Animals possessing a visual system can sense particular wavelengths of light emanating from objects and their surroundings and perceive their environments by processing information contained in these visual perceptions of light. Visual perception in individuals varies with the absorption spectra of visual pigments and the expression levels of opsin genes, which may be altered according to the light environments. However, which light environments and the mechanism by which they change opsin expression profiles and whether these changes in opsin gene expression can affect light sensitivities are largely unknown. This study determined whether the light environment during growth induced plastic changes in opsin gene expression and behavioral sensitivity to particular wavelengths of light in guppies (Poecilia reticulata). ResultsIndividuals grown under orange light exhibited a higher expression of long wavelength-sensitive (LWS) opsin genes and a higher sensitivity to 600-nm light than those grown under green light. In addition, we confirmed that variations in the expression levels of LWS opsin genes were related to the behavioral sensitivities to long wavelengths of light. Conclusions The light environment during the growth stage alters the expression levels of LWS opsin genes and behavioral sensitivities to long wavelengths of light in guppies. The plastically enhanced sensitivity to background light due to changes in opsin gene expression can enhance the detection and visibility of predators and foods, thereby affecting survival. Moreover, changes in sensitivities to orange light may lead to changes in the discrimination of orange/red colors of male guppies and might alter female preferences for male color patterns.
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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.
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A major goal of modern evolutionary biology is to understand the causes and consequences of phenotypic plasticity, the ability of a single genotype to produce multiple phenotypes in response to variable environments. While ecological and quantitative genetic studies have evaluated models of the evolution of adaptive plasticity, some long-standing questions about plasticity require more mechanistic approaches. Here, we address two of those questions: does plasticity facilitate adaptive evolution? And do physiological costs place limits on plasticity? We examine these questions by comparing genetically and plastically regulated behavioural variation in sailfin mollies (Poecilia latipinna), which exhibit striking variation in plasticity for male mating behaviour. In this species, some genotypes respond plastically to a change in the social environment by switching between primarily courting and primarily sneaking behaviour. In contrast, other genotypes have fixed mating strategies (either courting or sneaking) and do not display plasticity. We found that genetic and plastic variation in behaviour were accompanied by partially, but not completely overlapping changes in brain gene expression, in partial support of models that predict that plasticity can facilitate adaptive evolution. We also found that behavioural plasticity was accompanied by broader and more robust changes in brain gene expression, suggesting a substantial physiological cost to plasticity. We also observed that sneaking behaviour, but not courting, was associated with upregulation of genes involved in learning and memory, suggesting that sneaking is more cognitively demanding than courtship.
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Recent evidence shows that brain-derived steroids such as estrogens ("neuroestrogens") are controlled in a manner very similar to traditional neurotransmitters. The advent of in vivo microdialysis for steroids in songbirds has provided new information about the spatial and temporal dynamics of neuroestrogen changes in a region of the auditory cortex, the caudomedial nidopallium (NCM). Here, experiments using in vivo microdialysis demonstrate that neuroestradiol (E(2)) fluctuations occur within the auditory NCM during presentation of naturalistic auditory and visual stimuli in males but only to the presentation of auditory stimuli in females. These changes are acute (within 30 min) and appear to be specific to the NCM, because similar treatments elicit no changes in E(2) in a nearby mesopallial region or in circulating plasma. Further experiments coupling in vivo steroid microdialysis with extracellular recordings in NCM show that neuroestrogens rapidly boost auditory responses to song stimuli in females, similar to recent observations in males. We also find that the rapid actions of estradiol on auditory responses are fully mimicked by the cell membrane-impermeable estrogen biotinylestradiol, consistent with acute estrogen actions at the neuronal membrane. Thus we conclude that local and acute E(2) flux is regulated by convergent multimodal sensory input, and that this regulation appears to be sex-specific. Second, rapid changes in local E(2) levels in NCM have consequences for the modulation of auditory processing in females and males. Finally, the rapid actions of neuroestrogens on NCM auditory processing appear to be mediated by a nonclassical, membrane-bound estrogen receptor.
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Estrogens mediate profound effects throughout the body and regulate physiological and pathological processes in both women and men. The low prevalence of many diseases in premenopausal women is attributed to the presence of 17β-estradiol, the predominant and most potent endogenous estrogen. In addition to endogenous estrogens, several man-made and plant-derived molecules, such as bisphenol A and genistein, also exhibit estrogenic activity. Traditionally, the actions of 17β-estradiol are ascribed to two nuclear estrogen receptors (ERs), ERα and ERβ, which function as ligand-activated transcription factors. However, 17β-estradiol also mediates rapid signaling events via pathways that involve transmembrane ERs, such as G-protein-coupled ER 1 (GPER; formerly known as GPR30). In the past 10 years, GPER has been implicated in both rapid signaling and transcriptional regulation. With the discovery of GPER-selective ligands that can selectively modulate GPER function in vitro and in preclinical studies and with the use of Gper knockout mice, many more potential roles for GPER are being elucidated. This Review highlights the physiological roles of GPER in the reproductive, nervous, endocrine, immune and cardiovascular systems, as well as its pathological roles in a diverse array of disorders including cancer, for which GPER is emerging as a novel therapeutic target and prognostic indicator.
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In social species animals should fine-tune the expression of their social behavior to social environments in order to avoid the costs of engaging in costly social interactions. Therefore, social competence, defined as the ability of an animal to optimize the expression of its social behavior as a function of the available social information, should be considered as a performance trait that impacts on the Darwinian fitness of the animal. Social competence is based on behavioral plasticity which, in turn, can be achieved by different neural mechanisms of plasticity, namely by rewiring or by biochemically switching nodes of a putative neural network underlying social behavior. Since steroid hormones respond to social interactions and have receptors extensively expressed in the social behavioral neural network, it is proposed that steroids play a key role in the hormonal modulation of social plasticity. Here, we propose a reciprocal model for the action of androgens on short-term behavioral plasticity and review a set of studies conducted in our laboratory using an African cichlid fish (Oreochromis mossambicus) that provide support for it. Androgens are shown to be implicated as physiological mediators in a wide range of social phenomena that promote social competence, namely by adjusting the behavioral response to the nature of the intruder and the presence of third parties (dear enemy and audience effects), by anticipating territorial intrusions (bystander effect and conditioning of the territorial response), and by modifying future behavior according to prior experience of winning (winner effect). The rapid behavioral actions of socially induced short-term transient changes in androgens indicate that these effects are most likely mediated by nongenomic mechanisms. The fact that the modulation of rapid changes in behavior is open to the influence of circulating levels of androgens, and is not exclusively achieved by changes in central neuromodulators, suggests functional relevance of integrating body parameters in the behavioral response. Thus, the traditional view of seeing neural circuits as unique causal agents of behavior should be updated to a brain-body-environment perspective, in which these neural circuits are embodied and the behavioral performance (and outcomes as fitness) depends on a dynamic relationship between the different levels. In this view hormones play a major role as behavioral modulators.
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Female preference for male orange coloration in the genus Poecilia suggests a role for duplicated long wavelength-sensitive (LWS) opsin genes in facilitating behaviors related to mate choice in these species. Previous work has shown that LWS gene duplication in this genus has resulted in expansion of long wavelength visual capacity as determined by microspectrophotometry (MSP). However, the relationship between LWS genomic repertoires and expression of LWS retinal cone classes within a given species is unclear. Our previous study in the related species, Xiphophorus helleri, was the first characterization of the complete LWS opsin genomic repertoire in conjunction with MSP expression data in the family Poeciliidae, and revealed the presence of four LWS loci and two distinct LWS cone classes. In this study we characterized the genomic organization of LWS opsin genes by BAC clone sequencing, and described the full range of cone cell types in the retina of the colorful Cumaná guppy, Poecilia reticulata. In contrast to X. helleri, MSP data from the Cumaná guppy revealed three LWS cone classes. Comparisons of LWS genomic organization described here for Cumaná to that of X. helleri indicate that gene divergence and not duplication was responsible for the evolution of a novel LWS haplotype in the Cumaná guppy. This lineage-specific divergence is likely responsible for a third additional retinal cone class not present in X. helleri, and may have facilitated the strong sexual selection driven by female preference for orange color patterns associated with the genus Poecilia.
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Sexual harassment by males has been reported from several live-bearing fishes (Poeciliidae) and has been shown to inflict costs on females. For example, poeciliid females have reduced feeding opportunities when accompanied by a male because females dedicate attention to avoiding male copulation attempts. Poeciliid species differ considerably in male mating behavior, such as the presence or absence of courtship. Courting males display in front of the females, but males attempting to sneak-copulate approach females from behind, that is, in the blind portion of their visual field, and force copulations, which can be viewed as a male persistence trait. We predicted that poeciliid females need to be more vigilant in the presence of noncourting males, and costs of harassment by noncourting males might be stronger. In a comparative approach we examined the costs of male sexual harassment for females as reduced feeding time in 9 species of live-bearing fishes, including courting (Poecilia latipinna, Poecilia reticulata, Xiphophorus cortezi, Xiphophorus variatus) and noncourting species (Poecilia mexicana [surface- and cave-dwelling form], Poecilia orri, Gambusia affinis, Gambusia geiseri, Heterandria formosa). In all species examined except for the cave form of P. mexicana, focal females spent significantly less time feeding in the presence of a male than when together with another female. The time females spent feeding was found to significantly decline with increasing male mating activity (sum of all sexual behaviors), but there was no support for the idea that females would spend more time feeding in the presence of courting males compared with noncourting ones.
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Coloration and color vision covary with lighting in many taxa. Determining the mechanisms underlying these patterns is difficult because lighting environments can have multiple effects on signaling that occur at multiple timescales. Lighting environments can (1) immediately affect signal propagation and transmission, which determine the radiance spectrum reaching the receiver; (2) induce variation in visual systems via developmental plasticity; and (3) lead to genetic differences in visual systems due to a history of selection in different habitats. We tease apart these effects on pecking preference and examine the relationship between pecking preference and opsin expression. Using killifish from two visually distinct populations (clear vs. tea-stained water), we performed crosses (genetics), raised animals under different lighting conditions (developmental plasticity), and assayed the preference to peck at different-colored dots under different lighting conditions (immediate effects). Pecks are interpreted as foraging preference. Developmental plasticity affected both pecking preference and opsin expression. Lighting environments also had immediate effects on pecking preference, but these depended on the lighting conditions animals experienced during development. Genetic effects were detected in opsin expression, but there were no corresponding effects on pecking preference. Overall, only 3.36% of the variation in pecking preference was accounted for by opsin expression.
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Estrogens rapidly regulate neuronal activity within seconds-to-minutes, yet it is unclear how estrogens interact with neural circuits to rapidly coordinate behavior. This study examines whether 17-beta-estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal control circuit. Adult plainfin midshipman fish emit vocalizations that mainly differ in duration, and rhythmic activity of a hindbrain-spinal vocal pattern generator (VPG) directly establishes the temporal features of midshipman vocalizations. VPG activity is therefore predictive of natural calls, and 'fictive calls' can be elicited by electrical microstimulation of the VPG. Prior studies show that intramuscular estradiol injection rapidly (within 5 min) increases fictive call duration in midshipman. Here, we delivered opioid antagonists near the VPG prior to estradiol injection. Rapid estradiol actions on fictive calling were completely suppressed by the broad-spectrum opioid antagonist naloxone and the mu-opioid antagonist beta-funaltrexamine, but were unaffected by the kappa-opioid antagonist nor-binaltorphimine. Unexpectedly, prior to estradiol administration, all three opioid antagonists caused immediate, transient reductions in fictive call duration. Together, our results indicate that: (1) vocal activity is modulated by opioidergic networks, confirming hypotheses from birds and mammals, and (2) the rapid actions of estradiol on vocal patterning depend on interactions with a mu-opioid modulatory network.
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A major goal of evolutionary biology is to unravel the molecular genetic mechanisms that underlie functional diversification and adaptation. We investigated how changes in gene regulation and coding sequence contribute to sensory diversification in two replicate radiations of cichlid fishes. In the clear waters of Lake Malawi, differential opsin expression generates diverse visual systems, with sensitivities extending from the ultraviolet to the red regions of the spectrum. These sensitivities fall into three distinct clusters and are correlated with foraging habits. In the turbid waters of Lake Victoria, visual sensitivity is constrained to longer wavelengths, and opsin expression is correlated with ambient light. In addition to regulatory changes, we found that the opsins coding for the shortest- and longest-wavelength visual pigments have elevated numbers of potentially functional substitutions. Thus, we present a model of sensory evolution in which both molecular genetic mechanisms work in concert. Changes in gene expression generate large shifts in visual pigment sensitivity across the collective opsin spectral range, but changes in coding sequence appear to fine-tune visual pigment sensitivity at the short- and long-wavelength ends of this range, where differential opsin expression can no longer extend visual pigment sensitivity.
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Across all major vertebrate groups, androgen receptors (ARs) have been identified in neural circuits that shape reproductive-related behaviors, including vocalization. The vocal control network of teleost fishes presents an archetypal example of how a vertebrate nervous system produces social, context-dependent sounds. We cloned a partial cDNA of AR that was used to generate specific probes to localize AR expression throughout the central nervous system of the vocal plainfin midshipman fish (Porichthys notatus). In the forebrain, AR mRNA is abundant in proposed homologs of the mammalian striatum and amygdala, and in anterior and posterior parvocellular and magnocellular nuclei of the preoptic area, nucleus preglomerulosus, and posterior, ventral and anterior tuberal nuclei of the hypothalamus. Many of these nuclei are part of the known vocal and auditory circuitry in midshipman. The midbrain periaqueductal gray, an essential link between forebrain and hindbrain vocal circuitry, and the lateral line recipient nucleus medialis in the rostral hindbrain also express abundant AR mRNA. In the caudal hindbrain-spinal vocal circuit, high AR mRNA is found in the vocal prepacemaker nucleus and along the dorsal periphery of the vocal motor nucleus congruent with the known pattern of expression of aromatase-containing glial cells. Additionally, abundant AR mRNA expression is shown for the first time in the inner ear of a vertebrate. The distribution of AR mRNA strongly supports the role of androgens as modulators of behaviorally defined vocal, auditory, and neuroendocrine circuits in teleost fish and vertebrates in general.
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Pacific salmonids start life in fresh water then migrate to the sea, after a metamorphic event called smoltification, later returning to their natal freshwater streams to spawn and die. To accommodate changes in visual environments throughout life history, salmon may adjust their spectral sensitivity. We investigated this possibility by examining ontogenetic and thyroid hormone (TH)-induced changes in visual pigments in coho salmon (Oncorhynchus kisutch, Walbaum). Using microspectrophotometry, we measured the spectral absorbance (quantified by lambda(max)) of rods, and middle and long wavelength-sensitive (MWS and LWS) cones in three age classes of coho, representing both freshwater and marine phases. The lambda(max) of MWS and LWS cones differed among freshwater (alevin and parr) and ocean (smolt) phases. The lambda(max) of rods, on the other hand, did not vary, which is evidence that vitamin A(1)/A(2) visual pigment chromophore ratios were similar among freshwater and ocean phases when sampled at the same time of year. Exogenous TH treatment long wavelength shifted the lambda(max) of rods, consistent with an increase in A(2). However, shifts in cones were greater than predicted for a change in chromophore ratio. Real-time quantitative RT-PCR demonstrated that at least two RH2 opsin subtypes were expressed in MWS cones, and these were differentially expressed among alevin, parr and TH-treated alevin groups. Combined with changes in A(1)/A(2) ratio, differential expression of opsin subtypes allows coho to alter the spectral absorbance of their MWS and LWS cones by as much as 60 and 90 nm, respectively. To our knowledge, this is the largest spectral shift reported in a vertebrate photoreceptor.
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Phenotypic plasticity plays an important role in adapting the visual capability of many animal species to changing sensory requirements. Such variability may be driven by developmental change or may result from environmental changes in light habitat, thereby improving performance in different photic environments. In this study, we examined inter- and intraspecific plasticity of visual sensitivities in seven damselfish species; part of the species-rich and colorful fish fauna of the Great Barrier Reef in Australia. Our goal was to test whether the visual systems of damselfish were tuned to the prevailing light environment in different habitats and/or other aspects of their life style. More specifically, we compared the opsin gene expression levels from individuals living in different photic habitats. We found that all species expressed rod opsin (RH1) used for dim light vision, and primarily three cone opsins (SWS1, RH2B and RH2A) used for color vision. While RH1 levels changed exclusively following a diurnal cycle, cone opsin expression varied with depth in four of the seven species. Estimates of visual pigment performance imply that changes in opsin expression adjust visual sensitivities to the dominant photic regime. However, we also discovered that some species show a more stable opsin expression profile. Further, we found indication that seasonal changes, possibly linked to changes in the photic environment, might also trigger opsin expression. These findings suggest that plasticity in opsin gene expression of damselfish is highly species-specific, possibly due to ecological differences in visual tasks or, alternatively, under phylogenetic constraints. This article is protected by copyright. All rights reserved.
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We cloned the cDNAs corresponding to three oestrogen receptors (ERs) in zebrafish (Danio rerio). Sequence analysis and phylogenetic studies demonstrated that two of these genes, ER beta.1 and ER beta.2, arose from duplication of the original ER beta in many species of the fish phylum, whereas ER alpha is unique. Zebrafish ERs behaved as oestrogen-dependent transcription factors in transactivation assays. However, their reactivity to various oestrogen modulators was different compared with that of mouse ERs. ER mRNA expression during zebrafish development is restricted to distinct time periods, as observed by RNase protection assays. ER beta.2 is initially expressed as maternally transmitted RNA, until 6 h after fertilization, when expression disappears. Between 6 and 48 h after fertilization, no ER expression could be observed. After 48 h after fertilization, all ERs, but predominantly ER alpha, began to be expressed. We conclude that oestrogen signal transduction can operate during zebrafish development only within discrete time windows.
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Antiestrogens such as tamoxifen are one of the most effective methods of treating estrogen receptor (ERα) positive breast cancers; however, the effectiveness of this therapy is limited by the almost universal development of resistance to the drug. If antiestrogens are recognized differently by the cell as it has been suggested, then in disease conditions where tamoxifen fails to function effectively, a mechanistically different antiestrogen might yield successful results. Although many antiestrogens have been developed, a direct comparison of their mechanisms of action is lacking, thus limiting their utility. Therefore, to determine if there are mechanistic differences among available antiestrogens, we have carried out a comprehensive analysis of the molecular mechanisms of action of 4-hydroxy-tamoxifen (4OHT), idoxifene, raloxifene, GW7604, and ICI 182,780. Using a novel set of peptides that recognize different surfaces on ERα, we have found that following binding to ERα, each ligand induces a distinct ERα-ligand conformation. Furthermore, transcriptional assays indicate that each ERα-ligand complex is recognized distinctly by the transcription machinery, and consequently, antiestrogens vary in their ability to inhibit estradiol- and 4OHT-mediated activities. Relative binding assays have shown that the affinity of these ligands for ERα is not always representative of their inhibitory activity. Using this assay, we have also shown that the pharmacology of each antiestrogen is influenced differently by hormone binding proteins. Furthermore, GW7604, like ICI 182,780, but unlike the other antiestrogens evaluated, decreases the stability of the receptor. Overall, our results indicate that there are clear mechanistic distinctions among each of the antiestrogens studied. However, GW7604 and ICI 182,780 differ more significantly from tamoxifen than idoxifene and raloxifene. These data, which reveal differences among antiestrogens, should assist in the selection of compounds for the clinical regulation of ERα function.
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A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for co-variation in visual tuning, light environment, and mate preferences. Female preference co-evolves with male coloration, such that guppy females from ‘low predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high predation’ environments. Here we show that color vision also varies across populations, with ‘low’ predation guppies investing more of their color vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS-1 and LWS-3 (the most abundant LWS opsins) in ‘low predation’ populations than ‘high predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high and low predation populations. Together this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of variation in this model system.This article is protected by copyright. All rights reserved.
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Endocrine-disrupting chemicals (EDCs) are believed to interfere with animal reproduction, but only few biomarkers above the cellular level have been developed to assess the adverse effects of these chemicals. Using the guppy (Poecilia reticulata) as a model organism, studies have been undertaken with the object of comparing biomarker responses to EDCs at increasing levels of biological complexity. Short-term exposure to the xenoestrogen 4-tert-octylphenol and the natural estrogen 17beta-estradiol (E2) changed important sexual characteristics in the adult male guppy. Both compounds increased the number of sperm cells in the ejaculates, reduced the area and color intensity of the sexually attractive orange spots, and inhibited testis growth. In the case of E2, the effects on sperm count and coloration were still evident after 3 months of recovery in clean water. Preliminary results on male reproductive capability demonstrated that treated males produced fewer offspring than untreated fish, indicating an impairment of reproduction itself.
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Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species-level differences in female behavioral and brain molecular responses represent 'canalized' or 'plastic' traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole brain gene expression analyses of neuroserpin, egr-1, and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning-based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion-driven mating systems.
Article
It is well established that estrogen-like environmental chemicals interact with the ligand-binding site of estrogen receptors (ER) to disrupt transcriptional control of estrogen responsive targets. Here we investigate the possibility that estrogens also impact splicing decisions on estrogen responsive genes, such as that encoding ERα itself. Targeted PCR cloning was applied to identify six ERα mRNA variants in zebrafish. Sequencing revealed alternate use of transcription and translation start sites, multiple exon deletions, intron retention and alternate polyadenylation. As determined by quantitative (q)PCR, N-terminal mRNA variants predicting long (ERαL) and short (ERαS) isoforms were differentially expressed by tissue-type, sex, stage of development and estrogen exposure. Whereas ERαL mRNA was diffusely distributed in liver, brain, heart, eye, and gonads, ERαS mRNA was preferentially expressed in liver (female > male) and ovary. Neither ERαL nor ERαS transcripts varied significantly during development, but 17β-estradiol selectively increased accumulation of ERαS mRNA (∼170-fold by 120 hpf), an effect mimicked by bisphenol-A and diethylstilbestrol. Significantly, a C-truncated variant (ERαS-Cx) lacking most of the ligand binding and AF-2 domains was transcribed exclusively from the short isoform promoter and was similar to ERαS in its tissue-, stage- and estrogen inducible expression. These results support the idea that promoter choice and alternative splicing of the esr1 gene of zebrafish are part of the autoregulatory mechanism by which estrogen modulates subsequent ERα expression, and further suggest that environmental estrogens could exert some of their toxic effects by altering the relative abundance of structurally and functionally distinct ERα isoforms.
Article
It is now clear that estrogens are not just circulating reproductive hormones, but that they also have neurotransmitter-like properties in a wide range of brain circuits. The view of estrogens as intrinsic neuromodulators that shape behavior has been bolstered by a series of recent developments from multiple vertebrate model systems. Here, we review several recent findings from studies of songbirds showing how the identified neural circuits that govern auditory processing and sensorimotor integration are modulated by the local and acute production of estrogens. First, studies using in vivo microdialysis demonstrate that estrogens fluctuate in auditory cortex (30-min time bin resolution) when songbirds are hearing song and interacting with conspecifics. Second, estrogens rapidly boost the auditory-evoked activity of neurons in the same auditory cortical region, enhancing auditory processing. Third, local pharmacological blockade of estrogen signaling in this region impairs auditory neuronal responsiveness as well as behavioral song preferences. Fourth, the rapid estrogen actions that occur within the auditory cortex can propagate upstream (transsynaptically) to sensorimotor circuits to enhance the neural representation of song. Lastly, we present new evidence that the receptor for the rapid actions of estradiol is likely in neuronal membranes, and that traditional nuclear estrogen receptor agonists do not mimic these rapid actions. Broadly speaking, many of these findings are observed in both males and females, emphasizing the fundamental importance of estrogens in neural circuit function. Together, these and other emergent studies provide support for rapid, brain-derived estrogen signaling in regulating sensorimotor integration, learning and perception. This article is protected by copyright. All rights reserved.
Article
The effect of different doses of anti-estrogenic chemical was studied in a cichlid Oreochromis niloticus on mortality, growth, sexual development and sex differentiation. Percent mortality (5, 10 and 10) appeared to be dose-dependent. All groups of tamoxifen (TA) treated fishes exhibited significant growth as compared to the controlled fishes. Immature fishes treated with TA at 200 microg l(-1), showed lower gonado-somatic-index (GSI) (male 0.137; female 0.118) than control group (male 0.138; female 0.122) of fishes. Ovarian and testicular differentiation was adjudged by the appearance of the ovarian cavity (ovary) and the efferent (sperm) duct (testis), respectively. Sex and sexual maturity of individual fishes were determined using standard histological method. Tamoxifen treatment to the fry (yolk sac absorbed stage) of Oreochromis niloticus in the dose of 200 microg l(-1) for 60 days produced 90% males and 1% intersex population. Results suggested masculinizing action of tamoxifen reversing the sex of genetic female tilapia.
Article
Expansions in sensory systems usually require processes such as gene duplication and divergence, and thus evolve slowly. We evaluate a novel mechanism leading to rapid sensory repertoire expansion: hybrid-sensory expansion (HSE). HSE occurs when two species with differently tuned sensory systems form a hybrid, bringing together alleles from each of the parental species. In one generation, a sensory repertoire is created that is the sum of the variance between parental species. The Amazon molly presents a unique opportunity to test the HSE hypothesis in a "frozen" hybrid. We compared opsin sequences of the Amazon molly, Poecilia formosa, to those of the parental species. Both parental species are homozygous at the RH2-1 locus and each of the four long wavelength sensitive loci, while P.  formosa possess two different alleles at these loci; one matching each parental allele. Gene expression analysis showed P.  formosa use the expanded opsin repertoire that was the result of HSE. Additionally, behavioral tests revealed P.  formosa respond to colored stimuli in a manner similar or intermediate to the parental species P. mexicana and P. latipinna. Together these results strongly support the HSE hypothesis. Hybrid-sensory repertoire expansion is likely important in other hybrid species and in other sensory systems.
Article
Although estrogens are widely considered circulating "sex steroid hormones" typically associated with female reproduction, recent evidence suggests that estrogens can act as local modulators of brain circuits in both males and females. The functional implications of this newly characterized estrogen signaling system have begun to emerge. This essay summarizes evidence in support of the hypothesis that the rapid production of estrogens in brain circuits can drive acute changes in both the production and perception of acoustic communication behaviors. These studies have revealed two fundamental neurobiological concepts: (1) estrogens can be locally produced in brain circuits, independent of levels in nearby circuits and in the circulation and (2) estrogens can have very rapid effects within these brain circuits to modulate social vocalizations, acoustic processing, and sensorimotor integration. This vertebrate-wide span of research, including vocalizing fishes, amphibians, and birds, emphasizes the importance of comparative model systems in understanding principles of neurobiology.
Article
Abstract— We conducted laboratory experiments which demonstrated that three littoral zone fishes differentially selected among three macrophytes when seeking refuge from predation. In the presence of a predator (a juvenile Micropterus salmoides), mosquitofish (Gambusia holbrooki), sailfin mollies (Poecilia latipinna). and dollar sunfish (Lepomis marginatus) displayed ferential use of four tank areas containing patches of either Hydrilla verticillata, Potamogeton illinoensis, Panicum hemitomon, or no plants. Patterns habitat selection, and the consistency of these patterns among replicates, differed among the three fishes and among three plant-density treatments - natural (each macrophyte presented at its mean field density), equal (all three macrophytes at the same density), and control (no plants). Selection for H. verticillata by mosquitofish was significant for both the equal and natural treatments, and thus was not caused by differences in plant density alone. Sailfin mollies displayed significant selection for H. verticillata only in the natural plant-density treatments. Dollar sunfish showed less consistent habitat selection than either mosquitofish or sailfin mollies. Significant habitat selection was not found in the absence of a predator, and there was no evidence for lection among the tank areas in control treatments. Patterns of habitat selection by the three fishes in our laboratory study corresponded to observed habitat use in Lake Okeechobee.
Article
Male mosquitofish allocate a large proportion of their time budget to attempting to inseminate unreceptive females. Because females invest considerable time and energy in avoiding unwanted copulations, sexual harassment is expected to conflict with other activities such as foraging. We found that sexual harassment more than halved the foraging efficiency of the female in a task requiring the retrieval of food items scattered on the water surface. The presence of shoalmates relieved the female from harassment and foraging efficiency increased with the number of females in the group. Small males attempted to mate significantly more than large males, causing a greater reduction in the female's foraging efficiency. When several males competed for the same female, the larger, dominant male prevented all the other males from attempting to mate and so had fewer opportunities to attempt copulation. Harassment from solitary males appeared to be more costly, as females foraged more efficiently when chased by a group of males. Because male sexual activity has a large impact on a female's feeding efficiency and possibly on her survival and reproduction, sexual conflict is expected to be important in shaping association patterns of female mosquitofish with conspecifics of both sexes. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour
Article
Among poeciliid fish, male sexual harassment is often intense and is costly for females. In Gambusia holbrooki, sexual harassment can greatly reduce female foraging efficiency when an isolated female is harassed by a single male and these costs are negatively correlated with male length. However, when females are in groups, male harassment is diluted and female foraging efficiency increases. When several males compete for the same female, mating attempts are monopolized by the dominant male and female foraging efficiency also increases. We tested whether females actively vary their schooling behaviour with conspecifics according to the presence of a harassing male. Consistent with the predictions, we found that females swam closer to each other when a male was visible. When chased by a male, females approached a group of males, and when males of different size were available, they preferred to stay close to large males. These results suggest that female schooling behaviour is a flexible strategy and that male sexual harassment may represent an important factor influencing social aggregation in poeciliids.
Article
Intraventricular injection of two small doses of estradiol-17β-hemisuccinate in 50% ethanol resulted in an increase in average auditory evoked responses in Rana p. pipiens to tone bursts at 4 frequencies. Vehicle injections (50% ethanol) of the same amount, on the other hand, did not change, or reduced, the auditory evoked responses. These results suggest that estrogen can alter the response properties of midbrain auditory neurons in frogs.
Article
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.
Article
Tamoxifen is widely used in the treatment of breast cancer and can enter the aquatic environment in municipal wastewater. To evaluate potential effects on embryonic development of Japanese medaka, fertilized eggs were exposed to tamoxifen at 1-625μg/l for 14 days. Adverse effects on hatchability and time to hatching only occurred at 125 and 625μg/l. Reproductive effects were assessed by exposing adults for 21 days to the same dose range. At all concentrations tested, tamoxifen significantly increased plasma vitellogenin levels in males in a dose-dependent manner. Fecundity and fertility were detrimentally affected at 625μg/l. Additionally, F1 eggs were removed from tamoxifen-contaminated water to evaluate transgenerational effects. Hatchability was affected at 625μg/l but no morphological deformities were observed. A significant dose-dependent increase in the proportion of genotypic males occurred at all concentrations greater than 5μg/l.
Article
Light-induced shifts in cone frequency and opsin expression occur in many aquatic species. Yet little is known about how quickly animals can alter opsin expression and, thereby, track their visual environments. Similarly, little is known about whether adult animals can alter opsin expression or whether shifts in opsin expression are limited to critical developmental windows. We took adult wild-caught bluefin killifish (Lucania goodei) from three different lighting environments (spring, swamp and variable), placed them under two different lighting treatments (clear vs. tea-stained water) and monitored opsin expression over 4 weeks. We measured opsin expression for five previously described opsins (SWS1, SWS2B, SWS2A, RH2-1 and LWS) as well as RH2-2 which we discovered via 454 sequencing. We used two different metrics of opsin expression. We measured expression of each opsin relative to a housekeeping gene and the proportional expression of each opsin relative to the total pool of opsins. Population and lighting environment had large effects on opsin expression which were present at the earliest time points indicating rapid shifts in expression. The two measures of expression produced radically different patterns. Proportional measures indicated large effects of light on SWS1 expression, whereas relative measures indicated no such effect. Instead, light had large effects on the relative expression of SWS2B, RH2-2, RH2-1 and LWS. We suggest that proportional measures of opsin expression are best for making inferences about colour vision, but that measures relative to a housekeeping gene are better for making conclusions about which opsins are differentially regulated.
Article
Although nonclassical estrogen actions initiated at the cell surface have been described in many tissues, the identities of the membrane estrogen receptors (mERs) mediating these actions remain unclear. Here we show that GPR30, an orphan receptor unrelated to nuclear estrogen receptors, has all the binding and signaling characteristics of a mER. A high-affinity (dissociation constant 2.7 nm), limited capacity, displaceable, single binding site specific for estrogens was detected in plasma membranes of SKBR3 breast cancer cells that express GPR30 but lack nuclear estrogen receptors. Progesterone-induced increases and small interfering RNA-induced decreases in GPR30 expression in SKBR3 cells were accompanied by parallel changes in specific estradiol-17beta (E2) binding. Plasma membranes of human embryonic kidney 293 cells transfected with GPR30, but not those of untransfected cells, and human placental tissues that express GPR30 also displayed high-affinity, specific estrogen binding typical of mERs. E2 treatment of transfected cell membranes caused activation of a stimulatory G protein that is directly coupled to the receptor, indicating GPR30 is a G protein-coupled receptor (GPCR), and also increased adenylyl cyclase activity. The finding that the antiestrogens tamoxifen and ICI 182,780, and an environmental estrogen, ortho,para-dichlorodiphenyldichloroethylene (o,p'-DDE), have high binding affinities to the receptor and mimic the actions of E2 has important implications for both the development and treatment of estrogen-dependent breast cancer. GPR30 is structurally unrelated to the recently discovered family of GPCR-like membrane progestin receptors. The identification of a second distinct class of GPCR-like steroid membrane receptors suggests a widespread role for GPCRs in nonclassical steroid hormone actions.
Article
The expression of cone opsin genes is a primary determinant of the characteristics of colour vision. Interspecific variation in opsin expression is common in African cichlids. It is correlated with foraging among cichlids from Lake Malawi, and with ambient light environment among cichlids from Lake Victoria. In this study, we tested whether gene expression varied within species such that it might be important in contributing to divergence. We hypothesized that light attenuation with depth would be correlated with predictable changes in gene expression in Lake Malawi, and that this variation would tune visual sensitivities to match the ambient light environment. We observed significant differences in cone opsin expression in three different comparisons among populations of the same species. Higher LWS expression was found in shallow versus deep Copadichromis eucinostomus. In Metriaclima zebra, individuals from Zimbawe Rock expressed significantly more SWS2B than those from Thumbi West Island, although these locales have similar ambient light environments. Finally, Tropheops gracilior from deeper water had significantly more variation in expression than their shallow counterparts. These results support that gene expression varies significantly between populations of the same species. Surprisingly, these results could not be explained by predicted visual performance as models predicted that differential expression patterns did not confer sensitivity advantages at different depths. This suggested that expression variation did not confer a local sensitivity advantage. Therefore, our findings were contrary to a primary requirement of the sensory bias hypothesis. As such, other explanations for intraspecific gene expression variation need to be tested.
Article
Sensory systems play crucial roles in survival and reproduction. Therefore, sensory plasticity has important evolutionary implications. In this study, we examined retinal plasticity in five species of cichlid fish from Lake Malawi. We compared the cone opsin expression profiles of wild-caught fish to lab-reared F(1) that had been raised in a UV minus, reduced intensity light environment. All of the opsin genes that were expressed in wild-caught fish were also expressed in lab-reared individuals. However, we found statistically significant differences in relative opsin expression among all five species. The most consistent difference was in the SWS2B (violet) opsin, which was always expressed at higher levels in lab-reared individuals. Estimates of visual pigment quantum catch suggest that this change in expression would increase retinal sensitivity in the light environment of the lab. We also found that the magnitude of plasticity varied across species. These findings have important implications for understanding the genetic regulation of opsin expression and raise many interesting questions about how the cichlid visual system develops. They also suggest that sensory plasticity may have facilitated the ecological diversification of cichlids in Lake Malawi.