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1.
Sci Rep ; 13(1): 12028, 2023 07 25.
Article in English | MEDLINE | ID: mdl-37491571

ABSTRACT

Animal sensory systems are tightly adapted to the demands of their environment. In the visual domain, research has shown that many species have circuits and systems that exploit statistical regularities in natural visual signals. The zebrafish is a popular model animal in visual neuroscience, but relatively little quantitative data is available about the visual properties of the aquatic habitats where zebrafish reside, as compared to terrestrial environments. Improving our understanding of the visual demands of the aquatic habitats of zebrafish can enhance the insights about sensory neuroscience yielded by this model system. We analyzed a video dataset of zebrafish habitats captured by a stationary camera and compared this dataset to videos of terrestrial scenes in the same geographic area. Our analysis of the spatiotemporal structure in these videos suggests that zebrafish habitats are characterized by low visual contrast and strong motion when compared to terrestrial environments. Similar to terrestrial environments, zebrafish habitats tended to be dominated by dark contrasts, particularly in the lower visual field. We discuss how these properties of the visual environment can inform the study of zebrafish visual behavior and neural processing and, by extension, can inform our understanding of the vertebrate brain.


Subject(s)
Visual Perception , Zebrafish , Animals , Visual Fields , Ecosystem , Brain
2.
Integr Comp Biol ; 63(2): 407-427, 2023 08 23.
Article in English | MEDLINE | ID: mdl-37263784

ABSTRACT

Pheromones are chemical signals that facilitate communication between animals, and most animals use pheromones for reproduction and other forms of social behavior. The identification of key ligands and olfactory receptors used for pheromonal communication provides insight into the sensory processing of these important cues. An individual's responses to pheromones can be plastic, as physiological status modulates behavioral outputs. In this review, we outline the mechanisms for pheromone sensation and highlight physiological mechanisms that modify pheromone-guided behavior. We focus on hormones, which regulate pheromonal communication across vertebrates including fish, amphibians, and rodents. This regulation may occur in peripheral olfactory organs and the brain, but the mechanisms remain unclear. While this review centers on research in fish, we will discuss other systems to provide insight into how hormonal mechanisms function across taxa.


Subject(s)
Pheromones , Smell , Animals , Pheromones/physiology , Smell/physiology , Hormones , Fishes , Perception
3.
Proc Natl Acad Sci U S A ; 120(1): e2214418120, 2023 01 03.
Article in English | MEDLINE | ID: mdl-36584295

ABSTRACT

Pheromones play essential roles in reproduction in many species. Prostaglandin F2α (PGF2α) acts as a female reproductive hormone and as a sex pheromone in some species. An olfactory receptor (OR) for PGF2α was recently discovered in zebrafish, but this signaling pathway is evolutionarily labile. To understand the evolution of signals that attract males to fertile females, we used the African cichlid Astatotilapia burtoni and found that adult males strongly prefer fertile female odors. Injection of a prostaglandin synthesis inhibitor abolishes this attractivity of fertile females, indicating these hormones are necessary for pheromonal signaling. Unlike zebrafish, A. burtoni males are insensitive to PGF2α, but they do exhibit strong preference for females injected with PGF2α. This attractiveness is independent of the PGF2α hormonal receptor Ptgfr, indicating that this pheromone signaling derives from PGF2α metabolization into a yet-undiscovered pheromone. We further discovered that fish that are insensitive to PGF2α lack an ortholog for the OR Or114 that zebrafish use to detect PGF2α. These results indicate that PGF2α itself does not directly induce male preference in cichlids. Rather, it plays a vital role that primes females to become attractive via an alternative male OR.


Subject(s)
Cichlids , Receptors, Odorant , Animals , Female , Male , Zebrafish , Hormones , Signal Transduction , Pheromones , Prostaglandins
4.
Curr Biol ; 32(23): 5008-5021.e8, 2022 12 05.
Article in English | MEDLINE | ID: mdl-36327979

ABSTRACT

Animals benefit from knowing if and how they are moving. Across the animal kingdom, sensory information in the form of optic flow over the visual field is used to estimate self-motion. However, different species exhibit strong spatial biases in how they use optic flow. Here, we show computationally that noisy natural environments favor visual systems that extract spatially biased samples of optic flow when estimating self-motion. The performance associated with these biases, however, depends on interactions between the environment and the animal's brain and behavior. Using the larval zebrafish as a model, we recorded natural optic flow associated with swimming trajectories in the animal's habitat with an omnidirectional camera mounted on a mechanical arm. An analysis of these flow fields suggests that lateral regions of the lower visual field are most informative about swimming speed. This pattern is consistent with the recent findings that zebrafish optomotor responses are preferentially driven by optic flow in the lateral lower visual field, which we extend with behavioral results from a high-resolution spherical arena. Spatial biases in optic-flow sampling are likely pervasive because they are an effective strategy for determining self-motion in noisy natural environments.


Subject(s)
Optic Flow , Animals , Zebrafish , Swimming
5.
R Soc Open Sci ; 9(4): 220077, 2022 Apr.
Article in English | MEDLINE | ID: mdl-35601449

ABSTRACT

Identifying genetic loci underlying trait variation provides insights into the mechanisms of diversification, but demonstrating causality and characterizing the role of genetic loci requires testing candidate gene function, often in non-model species. Here we establish CRISPR/Cas9 editing in Astatotilapia calliptera, a generalist cichlid of the remarkably diverse Lake Malawi radiation. By targeting the gene oca2 required for melanin synthesis in other vertebrate species, we show efficient editing and germline transmission. Gene edits include indels in the coding region, probably a result of non-homologous end joining, and a large deletion in the 3' untranslated region due to homology-directed repair. We find that oca2 knock-out A. calliptera lack melanin, which may be useful for developmental imaging in embryos and studying colour pattern formation in adults. As A. calliptera resembles the presumed generalist ancestor of the Lake Malawi cichlids radiation, establishing genome editing in this species will facilitate investigating speciation, adaptation and trait diversification in this textbook radiation.

6.
Sci Rep ; 11(1): 15138, 2021 07 23.
Article in English | MEDLINE | ID: mdl-34302019

ABSTRACT

Direct tests of gene function have historically been performed in a limited number of model organisms. The CRISPR/Cas system is species-agnostic, offering the ability to manipulate genes in a range of models, enabling insights into evolution, development, and physiology. Astatotilapia burtoni, a cichlid fish from the rivers and shoreline around Lake Tanganyika, has been extensively studied in the laboratory to understand evolution and the neural control of behavior. Here we develop protocols for the creation of CRISPR-edited cichlids and create a broadly useful mutant line. By manipulating the Tyrosinase gene, which is necessary for eumelanin pigment production, we describe a fast and reliable approach to quantify and optimize gene editing efficiency. Tyrosinase mutants also remove a major obstruction to imaging, enabling visualization of subdermal structures and fluorophores in situ. These protocols will facilitate broad application of CRISPR/Cas9 to studies of cichlids as well as other non-traditional model aquatic species.


Subject(s)
CRISPR-Cas Systems/genetics , Cichlids/genetics , Monophenol Monooxygenase/genetics , Animals , Evolution, Molecular , Gene Editing/methods , Lakes , Phenotype , Tanzania
7.
Proc Natl Acad Sci U S A ; 117(45): 28167-28174, 2020 11 10.
Article in English | MEDLINE | ID: mdl-33106426

ABSTRACT

Social hierarchies are ubiquitous in social species and profoundly influence physiology and behavior. Androgens like testosterone have been strongly linked to social status, yet the molecular mechanisms regulating social status are not known. The African cichlid fish Astatotilapia burtoni is a powerful model species for elucidating the role of androgens in social status given their rich social hierarchy and genetic tractability. Dominant A. burtoni males possess large testes and bright coloration and perform aggressive and reproductive behaviors while nondominant males do not. Social status in A. burtoni is in flux, however, as males alter their status depending on the social environment. Due to a teleost-specific whole-genome duplication, A. burtoni possess two androgen receptor (AR) paralogs, ARα and ARß, providing a unique opportunity to disentangle the role of gene duplication in the evolution of social systems. Here, we used CRISPR/Cas9 gene editing to generate AR mutant A. burtoni and performed a suite of experiments to interrogate the mechanistic basis of social dominance. We find that ARß, but not ARα, is required for testes growth and bright coloration, while ARα, but not ARß, is required for the performance of reproductive behavior and aggressive displays. Both receptors are required to reduce flees from females and either AR is sufficient for attacking males. Thus, social status in A. burtoni is inordinately dissociable and under the modular control of two AR paralogs. This type of nonredundancy may be important in facilitating social plasticity in A. burtoni and other species whose social status relies on social experience.


Subject(s)
Cichlids , Gene Expression Regulation , Social Dominance , Androgens/metabolism , Animals , CRISPR-Cas Systems , Cichlids/genetics , Cichlids/physiology , Female , Gene Editing , Gene Expression Regulation/genetics , Gene Expression Regulation/physiology , Male , Mutation , Receptors, Androgen/genetics , Receptors, Androgen/physiology , Social Behavior
8.
BMC Genomics ; 17(1): 835, 2016 10 26.
Article in English | MEDLINE | ID: mdl-27784286

ABSTRACT

BACKGROUND: The East African riverine cichlid species Astatotilapia burtoni serves as an important laboratory model for sexually dimorphic physiology and behavior, and also serves as an outgroup species for the explosive adaptive radiations of cichlid species in Lake Malawi and Lake Victoria. An astounding diversity of genetic sex determination systems have been revealed within the adaptive radiation of East African cichlids thus far, including polygenic sex determination systems involving the epistatic interaction of multiple, independently segregating sex determination alleles. However, sex determination has remained unmapped in A. burtoni. Here we present mapping results supporting the presence of multiple, novel sex determination alleles, and thus the presence of polygenic sex determination in A. burtoni. RESULTS: Using mapping in small families in conjunction with restriction-site associated DNA sequencing strategies, we identify associations with sex at loci on linkage group 13 and linkage group 5-14. Inheritance patterns support an XY sex determination system on linkage group 5-14 (a chromosome fusion relative to other cichlids studied), and an XYW system on linkage group 13, and these associations are replicated in multiple families. Additionally, combining our genetic data with comparative genomic analysis identifies another fusion that is unassociated with sex, with linkage group 8-24 and linkage group 16-21 fused in A. burtoni relative to other East African cichlid species. CONCLUSIONS: We identify genetic signals supporting the presence of three previously unidentified sex determination alleles at two loci in the species A. burtoni, strongly supporting the presence of polygenic sex determination system in the species. These results provide a foundation for future mapping of multiple sex determination genes and their interactions. A better understanding of sex determination in A. burtoni provides important context for their use in behavioral studies, as well as studies of the evolution of genetic sex determination and sexual conflicts in East African cichlids.


Subject(s)
Cichlids/genetics , Genetic Association Studies , Inheritance Patterns , Sex Determination Processes/genetics , Animals , Evolution, Molecular , Female , Genetic Linkage , Male , Penetrance , Polymorphism, Single Nucleotide , Sex Ratio
9.
J Exp Biol ; 219(Pt 24): 3861-3865, 2016 12 15.
Article in English | MEDLINE | ID: mdl-27742893

ABSTRACT

Dopamine regulates reproduction in part by modulating neuronal activity within the hypothalamic-pituitary-gonadal (HPG) axis. Previous studies suggested numerous mechanisms by which dopamine exerts inhibitory control over the HPG axis, ultimately changing the levels of sex steroids that regulate reproductive behaviors. However, it is not known whether these mechanisms are conserved across vertebrate species. In particular, it is unknown whether mechanisms underlying dopaminergic control of reproduction are shared between mammals and teleost fish. In mammals, dopamine directly inhibits gonadotropin-releasing hormone (GnRH1) hypothalamic neurons, the gatekeepers for activation of the HPG axis. Here, we demonstrate, for the first time in teleost fish, dopaminergic control of GnRH1 neurons via direct dopamine type-2-like receptor (D2R)-mediated inhibition within the hypothalamus. These results suggest that direct dopaminergic control of GnRH1 neurons via interactions in the hypothalamus is not exclusive to tetrapod reproductive control, but is likely conserved across vertebrate species.


Subject(s)
Cichlids/physiology , Dopamine/pharmacology , Gonadotropin-Releasing Hormone/metabolism , Neurons/metabolism , Action Potentials/drug effects , Action Potentials/physiology , Animals , Female , Male , Neurons/drug effects , Preoptic Area/drug effects , Preoptic Area/enzymology , Receptors, Dopamine D1/metabolism , Receptors, Dopamine D2/metabolism , Sex Characteristics , Tyrosine 3-Monooxygenase/metabolism
10.
Curr Biol ; 26(7): 943-9, 2016 Apr 04.
Article in English | MEDLINE | ID: mdl-26996507

ABSTRACT

In most species, females time reproduction to coincide with fertility. Thus, identifying factors that signal fertility to the brain can provide access to neural circuits that control sexual behaviors. In vertebrates, levels of key signaling molecules rise at the time of fertility to prime the brain for reproductive behavior [1-11], but how and where they regulate neural circuits is not known [12, 13]. Specifically, 17α,20ß-dihydroxyprogesterone (DHP) and prostaglandin F2α (PGF2α) levels rise in teleost fish around the time of ovulation [10, 14, 15]. In an African cichlid fish, Astatotilapia burtoni, fertile females select a mate and perform a stereotyped spawning routine, offering quantifiable behavioral outputs of neural circuits. We show that, within minutes, PGF2α injection activates a naturalistic pattern of sexual behavior in female A. burtoni. We also identify cells in the brain that transduce the prostaglandin signal to mate and show that the gonadal steroid DHP modulates mRNA levels of the putative receptor for PGF2α (Ptgfr). We use CRISPR/Cas9 to generate the first targeted gene mutation in A. burtoni and show that Ptgfr is necessary for the initiation of sexual behavior, uncoupling sexual behavior from reproductive status. Our findings are consistent with a model in which PGF2α communicates fertility status via Ptgfr to circuits in the brain that drive female sexual behavior. Our targeted genome modification in a cichlid fish shows that dissection of gene function can reveal basic control mechanisms for behaviors in this large family of species with diverse and fascinating social systems [16, 17].


Subject(s)
Cichlids/physiology , Dinoprost/metabolism , Sexual Behavior, Animal , Signal Transduction , Animals , Female , Fish Proteins/genetics , Fish Proteins/metabolism , Male , Receptors, Prostaglandin/genetics , Receptors, Prostaglandin/metabolism
11.
Curr Opin Neurobiol ; 38: 57-62, 2016 06.
Article in English | MEDLINE | ID: mdl-26952366

ABSTRACT

Fish comprise half of extant vertebrate species and use a rich variety of reproductive strategies that have yielded insights into the basic mechanisms that evolved for sex. To maximize the chances of fertilization and survival of offspring, fish species time reproduction to occur at optimal times. For years, ethologists have performed painstaking experiments to identify sensory inputs and behavioral outputs of the brain during mating. Here we review known mechanisms that generate sexual behavior, focusing on the factors that govern the timing of these displays. The development of new technologies, including high-throughput sequencing and genome engineering, has the potential to provide novel insights into how the vertebrate brain consummates mating at the appropriate time.


Subject(s)
Fishes/physiology , Reproduction/physiology , Animals , Cues , Sexual Behavior, Animal/physiology
12.
Proc Natl Acad Sci U S A ; 112(12): 3805-10, 2015 Mar 24.
Article in English | MEDLINE | ID: mdl-25775522

ABSTRACT

Initiating and regulating vertebrate reproduction requires pulsatile release of gonadotropin-releasing hormone (GnRH1) from the hypothalamus. Coordinated GnRH1 release, not simply elevated absolute levels, effects the release of pituitary gonadotropins that drive steroid production in the gonads. However, the mechanisms underlying synchronization of GnRH1 neurons are unknown. Control of synchronicity by gap junctions between GnRH1 neurons has been proposed but not previously found. We recorded simultaneously from pairs of transgenically labeled GnRH1 neurons in adult male Astatotilapia burtoni cichlid fish. We report that GnRH1 neurons are strongly and uniformly interconnected by electrical synapses that can drive spiking in connected cells and can be reversibly blocked by meclofenamic acid. Our results suggest that electrical synapses could promote coordinated spike firing in a cellular assemblage of GnRH1 neurons to produce the pulsatile output necessary for activation of the pituitary and reproduction.


Subject(s)
Cichlids/physiology , Electrical Synapses , Gonadotropin-Releasing Hormone/metabolism , Animals , Connexins/metabolism , Female , Gap Junctions , Gene Regulatory Networks , Green Fluorescent Proteins/metabolism , In Situ Hybridization , Male , Meclofenamic Acid/chemistry , Models, Neurological , Neurons/physiology , Pituitary Gland/metabolism , Synaptic Transmission , Transgenes
13.
PLoS One ; 8(10): e77647, 2013.
Article in English | MEDLINE | ID: mdl-24204902

ABSTRACT

Cichlid fishes represent one of the most species-rich and rapid radiations of a vertebrate family. These ~2200 species, predominantly found in the East African Great Lakes, exhibit dramatic differences in anatomy, physiology, and behavior. However, the genetic bases for this radiation, and for the control of their divergent traits, are unknown. A flood of genomic and transcriptomic data promises to suggest mechanisms underlying the diversity, but transgenic technology will be needed to rigorously test the hypotheses generated. Here we demonstrate the successful use of the Tol2 transposon system to generate transgenic Astatotilapia burtoni, a haplochromine cichlid from Lake Tanganyika, carrying the GFP transgene under the control of the ubiquitous EF1α promoter. The transgene integrates into the genome, is successfully passed through the germline, and the widespread GFP expression pattern is stable across siblings and multiple generations. The stable inheritance and expression patterns indicate that the Tol2 system can be applied to generate A. burtoni transgenic lines. Transgenesis has proven to be a powerful technology for manipulating genes and cells in other model organisms and we anticipate that transgenic A. burtoni and other cichlids will be used to test the mechanisms underlying behavior and speciation.


Subject(s)
Animals, Genetically Modified/genetics , Cichlids/genetics , Genome/genetics , Animals , DNA Transposable Elements/genetics , Transgenes/genetics
14.
Cell ; 153(4): 896-909, 2013 May 09.
Article in English | MEDLINE | ID: mdl-23663785

ABSTRACT

Sexual dimorphisms in the brain underlie behavioral sex differences, but the function of individual sexually dimorphic neuronal populations is poorly understood. Neuronal sexual dimorphisms typically represent quantitative differences in cell number, gene expression, or other features, and it is unknown whether these dimorphisms control sex-typical behavior exclusively in one sex or in both sexes. The progesterone receptor (PR) controls female sexual behavior, and we find many sex differences in number, distribution, or projections of PR-expressing neurons in the adult mouse brain. Using a genetic strategy we developed, we have ablated one such dimorphic PR-expressing neuronal population located in the ventromedial hypothalamus (VMH). Ablation of these neurons in females greatly diminishes sexual receptivity. Strikingly, the corresponding ablation in males reduces mating and aggression. Our findings reveal the functions of a molecularly defined, sexually dimorphic neuronal population in the brain. Moreover, we show that sexually dimorphic neurons can control distinct sex-typical behaviors in both sexes.


Subject(s)
Aggression/physiology , Hypothalamus/metabolism , Neurons/metabolism , Sex Characteristics , Sexual Behavior , Animals , Female , Hypothalamus/cytology , Male , Mice , Mice, Inbred C57BL , Receptors, Progesterone/analysis , Receptors, Progesterone/metabolism , Sexual Behavior, Animal
15.
Neuron ; 66(2): 260-72, 2010 Apr 29.
Article in English | MEDLINE | ID: mdl-20435002

ABSTRACT

Testosterone and estrogen are essential for male behaviors in vertebrates. How these two signaling pathways interact to control masculinization of the brain and behavior remains to be established. Circulating testosterone activates the androgen receptor (AR) and also serves as the source of estrogen in the brain. We have used a genetic strategy to delete AR specifically in the mouse nervous system. This approach permits us to determine the function of AR in sexually dimorphic behaviors in males while maintaining circulating testosterone levels within the normal range. We find that AR mutant males exhibit masculine sexual and territorial displays, but they have striking deficits in specific components of these behaviors. Taken together with the surprisingly limited expression of AR in the developing brain, our findings indicate that testosterone acts as a precursor to estrogen to masculinize the brain and behavior, and signals via AR to control the levels of male behavioral displays.


Subject(s)
Brain/metabolism , Receptors, Androgen/metabolism , Sexual Behavior, Animal/physiology , Territoriality , Animals , Estrogens/metabolism , Male , Mice , Mice, Transgenic , Neurons/metabolism , Receptors, Androgen/genetics , Testosterone/metabolism
16.
Horm Behav ; 53(5): 627-37, 2008 May.
Article in English | MEDLINE | ID: mdl-18313055

ABSTRACT

It has been known since antiquity that gender-specific behaviors are regulated by the gonads. We now know that testosterone is required for the appropriate display of male patterns of behavior. Estrogen and progesterone, on the other hand, are essential for female typical responses. Research from several groups also indicates that estrogen signaling is required for male typical behaviors. This finding raises the issue of the relative contribution of these two hormonal systems in the control of male typical behavioral displays. In this review we discuss the findings that led to these conclusions and suggest various genetic strategies that may be required to understand the relative roles of testosterone and estrogen signaling in the control of gender-specific behavior.


Subject(s)
Androgens/genetics , Androgens/physiology , Behavior, Animal/physiology , Behavior/physiology , Estrogens/genetics , Estrogens/physiology , Animals , Female , Humans , Male , Receptors, Androgen/genetics , Receptors, Androgen/physiology , Receptors, Estrogen/genetics , Receptors, Estrogen/physiology , Sex Characteristics , Sexual Behavior, Animal/physiology
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