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Russell D. Fernald - One of the best experts on this subject based on the ideXlab platform.
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A behavioral logic underlying aggression in an African cichlid fish
2020Co-Authors: Beau A. Alward, Phillip H. Cathers, Danielle Blakkan, Russell D. FernaldAbstract:Social rank in a hierarchy determines which individuals have access to important resources such as food, shelter, and mates. In the African cichlid fish Astatotilapia Burtoni, rank is under social control, such that larger males are more likely than smaller males to be dominant in rank. Although it is well known that the relative size of A. Burtoni males is critical in controlling social rank, the specific behavioral strategies underlying responses to males of different sizes are not well understood. In this research, our goal was to characterize these responses by performing resident-intruder assays, in which aggressive behaviors were measured in territorial males in response to the introduction of unfamiliar males that differed in relative standard length (SL). We found that the relative SL of intruders played an important role in determining behavioral performance. Resident males exposed to larger (>5% larger in SL) or matched (between 0 and 5% larger or smaller in SL) intruder males performed more lateral displays, a type of non-physical aggression, compared to resident males exposed to smaller (>5% smaller in SL) intruder males. However, physical aggression, such as chases and bites, did not differ as a function of relative SL. Our results suggest that A. Burtoni males amplify non-physical aggression to settle territorial disputes in response to differences in relative SL that were not previously considered to be behaviorally relevant. HighlightsO_LIRelative size determines social rank in the African cichlid Astatotilapia Burtoni C_LIO_LIResident male A. Burtoni respond differently to small size differences in intruder males C_LIO_LIResidents perform more non-physical aggression against larger intruders C_LIO_LIResidents do not alter physical aggression as a function of differently sized intruders C_LIO_LIDistinct behavioral strategies are used against different intruders C_LI
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Modular genetic control of social status in a cichlid fish
2020Co-Authors: Beau A. Alward, Scott A. Juntti, Vibhav A. Laud, Christopher J. Skalnik, Ryan A. York, Russell D. FernaldAbstract:Social hierarchies are ubiquitous in social species, yet the mechanisms underlying social status are unclear. In the African cichlid fish Astatotilapia Burtoni, males stratify along a dominance hierarchy that varies based on testes mass, coloration, and behavior. Using androgen receptor (AR) mutant A. Burtoni generated using CRISPR/Cas9, we find that two AR genes control social dominance. ARβ, but not ARα, is required for testes growth and bright coloration, while ARα, but not ARβ, is required for the performance of reproductive behavior and aggressive displays. Neither receptor is required for attacking males. Analysis of AR double mutants revealed that either AR is sufficient for attacking males. Social status in A. Burtoni males is modularly controlled by ARα and ARβ, indicating that these genes have undergone subfunctionalization.
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Genome-wide effects of social status on DNA methylation in the brain of a cichlid fish, Astatotilapia Burtoni
BMC genomics, 2019Co-Authors: Austin T. Hilliard, Dan Xie, Michael Snyder, Russell D. FernaldAbstract:Successful social behavior requires real-time integration of information about the environment, internal physiology, and past experience. The molecular substrates of this integration are poorly understood, but likely modulate neural plasticity and gene regulation. In the cichlid fish species Astatotilapia Burtoni, male social status can shift rapidly depending on the environment, causing fast behavioral modifications and a cascade of changes in gene transcription, the brain, and the reproductive system. These changes can be permanent but are also reversible, implying the involvement of a robust but flexible mechanism that regulates plasticity based on internal and external conditions. One candidate mechanism is DNA methylation, which has been linked to social behavior in many species, including A. Burtoni. But, the extent of its effects after A. Burtoni social change were previously unknown. We performed the first genome-wide search for DNA methylation patterns associated with social status in the brains of male A. Burtoni, identifying hundreds of Differentially Methylated genomic Regions (DMRs) in dominant versus non-dominant fish. Most DMRs were inside genes supporting neural development, synapse function, and other processes relevant to neural plasticity, and DMRs could affect gene expression in multiple ways. DMR genes were more likely to be transcription factors, have a duplicate elsewhere in the genome, have an anti-sense lncRNA, and have more splice variants than other genes. Dozens of genes had multiple DMRs that were often seemingly positioned to regulate specific splice variants. Our results revealed genome-wide effects of A. Burtoni social status on DNA methylation in the brain and strongly suggest a role for methylation in modulating plasticity across multiple biological levels. They also suggest many novel hypotheses to address in mechanistic follow-up studies, and will be a rich resource for identifying the relationships between behavioral, neural, and transcriptional plasticity in the context of social status.
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Astatotilapia Burtoni: A Model System for Analyzing the Neurobiology of Behavior
ACS chemical neuroscience, 2018Co-Authors: Karen P. Maruska, Russell D. FernaldAbstract:Most biomedical research is performed using a very limited number of “model” species. In part, this has resulted from a combination of full genomes, manipulation of genes, and short generation times in these species. However, the advent of low-cost sequencing and gene editing in any organism has increased the use of nontraditional organisms. Many scientists have paraphrased the adage by Krogh [Krogh, A. (2018) Science 70, 200−204] that for many biological problems some species will prove to be most convenient and useful to study. In particular, using organisms most suited to the specific research question can lead to novel insights about fundamental physiological, neurobiological, immunological, and neuroendocrine systems that can advance our understanding of the well-being and health of humans. In addition, such studies have led to new ideas about the evolution and mechanisms that control social behavior. Fishes constitute about 50% of all vertebrate species and are the most diverse vertebrate radiation....
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Polygenic sex determination in the cichlid fish Astatotilapia Burtoni.
BMC genomics, 2016Co-Authors: Natalie B. Roberts, Russell D. Fernald, Scott A. Juntti, Kaitlin P. Coyle, Beth L. Dumont, M. Kaitlyn Stanley, Allyson Q. Ryan, Reade B. RobertsAbstract: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. 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. 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.
Karen P. Maruska - One of the best experts on this subject based on the ideXlab platform.
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Noise during mouthbrooding impairs maternal care behaviors and juvenile development and alters brain transcriptomes in the African cichlid fish Astatotilapia Burtoni.
Genes brain and behavior, 2020Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Anthropogenic noise has increased underwater ambient sound levels in the range in which most fishes detect and produce acoustic signals. Although the impacts of increased background noise on fish development have been studied in a variety of species, there is a paucity of information on how noise affects parental care. Mouthbrooding is an energetically costly form of parental care in which the brooding fish carries developing larvae in the buccal cavity for the duration of development. In the African cichlid Astatotilapia Burtoni, females carry their brood for ~2 weeks during which time they do not eat. To test the hypothesis that increased background noise impacts maternal care behaviors and brood development, we exposed brooding females to a 3-h period of excess noise (~140 dB) played through an underwater speaker. Over half of noise-exposed brooding females cannibalized or pre-maturely released their brood, but 90% of control females exhibited normal brooding behaviors. RNA-seq analysis revealed that transcripts related to feeding and parental care were differentially expressed in the brains of noise-exposed females. Juveniles that were exposed to noise during their brood period within the mother's mouth had lower body condition factors, higher mortality and altered head transcriptomes compared with control broods. Furthermore, onset of adult-typical coloration and behaviors was delayed compared with control fish. Together, these data indicate that noise has severe impacts on reproductive fitness in mouthbrooding females. Our results, combined with past studies, indicate that parental care stages are extremely susceptible to noise-induced perturbations with detrimental effects on species persistence.
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Female reproductive state is associated with changes in distinct arginine vasotocin cell types in the preoptic area of Astatotilapia Burtoni.
The Journal of comparative neurology, 2020Co-Authors: Julie M Butler, Chase M. Anselmo, Karen P. MaruskaAbstract:Nonapeptides play a crucial role in mediating reproduction, aggression, and parental care across taxa. In fishes, arginine vasotocin (AVT) expression is related to social and/or reproductive status in most male fishes studied to date, and is linked to territorial defense, paternal care, and courtship. Despite a plethora of studies examining AVT in male fishes, relatively little is known about how AVT expression varies with female reproductive state or its role in female social behaviors. We used multiple methods for examining the AVT system in female African cichlid fish Astatotilapia Burtoni, including immunohistochemistry for AVT, in situ hybridization for avt-mRNA, and quantitative PCR. Ovulated and mouthbrooding females had similar numbers of parvocellular, magnocellular, and gigantocellular AVT cells in the preoptic area. However, ovulated females had larger magnocellular and gigantocellular cells compared to mouthbrooding females, and gigantocellular AVT cell size correlated with the number of days brooding, such that late-stage brooding females had larger AVT cells than mid-stage brooding females. In addition, we found that ventral hypothalamic cells were more prominent in females compared to males, and were larger in mouthbrooding compared to ovulated females, suggesting a role in maternal care. Together, these data indicate that AVT neurons change across the reproductive cycle in female fishes, similar to that seen in males. These data on females complement studies in male A. Burtoni, providing a comprehensive picture of the regulation and potential function of different AVT cell types in reproduction and social behaviors in both sexes.
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Distribution of aromatase in the brain of the African cichlid fish Astatotilapia Burtoni: Aromatase expression, but not estrogen receptors, varies with female reproductive-state.
The Journal of comparative neurology, 2020Co-Authors: Karen P. Maruska, Julie M Butler, Chase M. Anselmo, Ganga TandukarAbstract:Estrogen synthesis and signaling in the brains of vertebrates has pleotropic effects ranging from neurogenesis to modulation of behaviors. The majority of studies on brain-derived estrogens focus on males, but estrogenic signaling in females likely plays important roles in regulation of reproductive cycling and social behaviors. We used females of the mouth brooding African cichlid fish, Astatotilapia Burtoni, to test for reproductive state-dependent changes in estrogenic signaling capacity within microdissected brain nuclei that are important for social behaviors. Expression levels of the rate-limiting enzyme aromatase, but not estrogen receptors, measured by qPCR changes across the reproductive cycle. Gravid females that are close to spawning had higher aromatase levels in all brain regions compared to females with lower reproductive potential. This brain aromatase expression was positively correlated with circulating estradiol levels and ovarian readiness. Using chromogenic in situ hybridization we localized aromatase-expressing cells to ependymal regions bordering the ventricles from the forebrain to the hindbrain, and observed more abundant staining in gravid compared to mouth brooding females in most regions. Staining was most prominent in subpallial telencephalic regions, and diencephalic regions of the preoptic area, thalamus, and hypothalamus, but was also observed in sensory and sensorimotor areas of the midbrain and hindbrain. Aromatase expression was observed in radial glial cells, revealed by co-localization with the glial marker GFAP and absence of co-localization with the neuronal marker HuC/D. Collectively these results support the idea that brain-derived estradiol in females may serve important functions in reproductive state-dependent physiological and behavioral processes across vertebrates.
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expression of tachykinin3 and related reproductive markers in the brain of the african cichlid fish Astatotilapia Burtoni
The Journal of Comparative Neurology, 2019Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Neurokinin B, encoded by the tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamic tac3 expression for its role in reproduction, but detailed studies on extra-hypothalamic tac3 expression are limited. Here, we identified two tac3 genes in the social African cichlid fish Astatotilapia Burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization for tac3a mRNA identified cell populations throughout the brain. Numerous tac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scattered tac3-expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts, tac3 expression was absent from the pituitary. Using double-fluorescent staining, we localized tac3a-expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH-tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse with tac3a cells in the preoptic area. Only minimal (<5%) colabeling of tac3a was observed in kiss2 cells. Despite tac3a expression in many nodes of the mesolimbic reward system, it was absent from tyrosine hydroxylase (TH)-expressing cells, but tac3a cells were located in areas with dense TH fibers. The presence of tac3a-expressing cells throughout the brain, including in socially relevant brain regions, suggest more diverse functions beyond regulation of reproductive physiology that may be conserved across vertebrates.
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Expression of tachykinin3 and related reproductive markers in the brain of the African cichlid fish Astatotilapia Burtoni.
The Journal of comparative neurology, 2019Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Neurokinin B, encoded by the tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamic tac3 expression for its role in reproduction, but detailed studies on extra-hypothalamic tac3 expression are limited. Here, we identified two tac3 genes in the social African cichlid fish Astatotilapia Burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization for tac3a mRNA identified cell populations throughout the brain. Numerous tac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scattered tac3-expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts, tac3 expression was absent from the pituitary. Using double-fluorescent staining, we localized tac3a-expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH-tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse with tac3a cells in the preoptic area. Only minimal (
Julie M Butler - One of the best experts on this subject based on the ideXlab platform.
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Noise during mouthbrooding impairs maternal care behaviors and juvenile development and alters brain transcriptomes in the African cichlid fish Astatotilapia Burtoni.
Genes brain and behavior, 2020Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Anthropogenic noise has increased underwater ambient sound levels in the range in which most fishes detect and produce acoustic signals. Although the impacts of increased background noise on fish development have been studied in a variety of species, there is a paucity of information on how noise affects parental care. Mouthbrooding is an energetically costly form of parental care in which the brooding fish carries developing larvae in the buccal cavity for the duration of development. In the African cichlid Astatotilapia Burtoni, females carry their brood for ~2 weeks during which time they do not eat. To test the hypothesis that increased background noise impacts maternal care behaviors and brood development, we exposed brooding females to a 3-h period of excess noise (~140 dB) played through an underwater speaker. Over half of noise-exposed brooding females cannibalized or pre-maturely released their brood, but 90% of control females exhibited normal brooding behaviors. RNA-seq analysis revealed that transcripts related to feeding and parental care were differentially expressed in the brains of noise-exposed females. Juveniles that were exposed to noise during their brood period within the mother's mouth had lower body condition factors, higher mortality and altered head transcriptomes compared with control broods. Furthermore, onset of adult-typical coloration and behaviors was delayed compared with control fish. Together, these data indicate that noise has severe impacts on reproductive fitness in mouthbrooding females. Our results, combined with past studies, indicate that parental care stages are extremely susceptible to noise-induced perturbations with detrimental effects on species persistence.
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Female reproductive state is associated with changes in distinct arginine vasotocin cell types in the preoptic area of Astatotilapia Burtoni.
The Journal of comparative neurology, 2020Co-Authors: Julie M Butler, Chase M. Anselmo, Karen P. MaruskaAbstract:Nonapeptides play a crucial role in mediating reproduction, aggression, and parental care across taxa. In fishes, arginine vasotocin (AVT) expression is related to social and/or reproductive status in most male fishes studied to date, and is linked to territorial defense, paternal care, and courtship. Despite a plethora of studies examining AVT in male fishes, relatively little is known about how AVT expression varies with female reproductive state or its role in female social behaviors. We used multiple methods for examining the AVT system in female African cichlid fish Astatotilapia Burtoni, including immunohistochemistry for AVT, in situ hybridization for avt-mRNA, and quantitative PCR. Ovulated and mouthbrooding females had similar numbers of parvocellular, magnocellular, and gigantocellular AVT cells in the preoptic area. However, ovulated females had larger magnocellular and gigantocellular cells compared to mouthbrooding females, and gigantocellular AVT cell size correlated with the number of days brooding, such that late-stage brooding females had larger AVT cells than mid-stage brooding females. In addition, we found that ventral hypothalamic cells were more prominent in females compared to males, and were larger in mouthbrooding compared to ovulated females, suggesting a role in maternal care. Together, these data indicate that AVT neurons change across the reproductive cycle in female fishes, similar to that seen in males. These data on females complement studies in male A. Burtoni, providing a comprehensive picture of the regulation and potential function of different AVT cell types in reproduction and social behaviors in both sexes.
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Distribution of aromatase in the brain of the African cichlid fish Astatotilapia Burtoni: Aromatase expression, but not estrogen receptors, varies with female reproductive-state.
The Journal of comparative neurology, 2020Co-Authors: Karen P. Maruska, Julie M Butler, Chase M. Anselmo, Ganga TandukarAbstract:Estrogen synthesis and signaling in the brains of vertebrates has pleotropic effects ranging from neurogenesis to modulation of behaviors. The majority of studies on brain-derived estrogens focus on males, but estrogenic signaling in females likely plays important roles in regulation of reproductive cycling and social behaviors. We used females of the mouth brooding African cichlid fish, Astatotilapia Burtoni, to test for reproductive state-dependent changes in estrogenic signaling capacity within microdissected brain nuclei that are important for social behaviors. Expression levels of the rate-limiting enzyme aromatase, but not estrogen receptors, measured by qPCR changes across the reproductive cycle. Gravid females that are close to spawning had higher aromatase levels in all brain regions compared to females with lower reproductive potential. This brain aromatase expression was positively correlated with circulating estradiol levels and ovarian readiness. Using chromogenic in situ hybridization we localized aromatase-expressing cells to ependymal regions bordering the ventricles from the forebrain to the hindbrain, and observed more abundant staining in gravid compared to mouth brooding females in most regions. Staining was most prominent in subpallial telencephalic regions, and diencephalic regions of the preoptic area, thalamus, and hypothalamus, but was also observed in sensory and sensorimotor areas of the midbrain and hindbrain. Aromatase expression was observed in radial glial cells, revealed by co-localization with the glial marker GFAP and absence of co-localization with the neuronal marker HuC/D. Collectively these results support the idea that brain-derived estradiol in females may serve important functions in reproductive state-dependent physiological and behavioral processes across vertebrates.
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expression of tachykinin3 and related reproductive markers in the brain of the african cichlid fish Astatotilapia Burtoni
The Journal of Comparative Neurology, 2019Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Neurokinin B, encoded by the tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamic tac3 expression for its role in reproduction, but detailed studies on extra-hypothalamic tac3 expression are limited. Here, we identified two tac3 genes in the social African cichlid fish Astatotilapia Burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization for tac3a mRNA identified cell populations throughout the brain. Numerous tac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scattered tac3-expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts, tac3 expression was absent from the pituitary. Using double-fluorescent staining, we localized tac3a-expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH-tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse with tac3a cells in the preoptic area. Only minimal (<5%) colabeling of tac3a was observed in kiss2 cells. Despite tac3a expression in many nodes of the mesolimbic reward system, it was absent from tyrosine hydroxylase (TH)-expressing cells, but tac3a cells were located in areas with dense TH fibers. The presence of tac3a-expressing cells throughout the brain, including in socially relevant brain regions, suggest more diverse functions beyond regulation of reproductive physiology that may be conserved across vertebrates.
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Expression of tachykinin3 and related reproductive markers in the brain of the African cichlid fish Astatotilapia Burtoni.
The Journal of comparative neurology, 2019Co-Authors: Julie M Butler, Karen P. MaruskaAbstract:Neurokinin B, encoded by the tachykinin3 gene, plays a crucial role in regulating reproduction in mammals via KNDy neurons and interaction with GnRH. Previous work in teleost fishes has focused on hypothalamic tac3 expression for its role in reproduction, but detailed studies on extra-hypothalamic tac3 expression are limited. Here, we identified two tac3 genes in the social African cichlid fish Astatotilapia Burtoni, only one of which produces a functional protein containing the signature tachykinin motif. In situ hybridization for tac3a mRNA identified cell populations throughout the brain. Numerous tac3a cells lie in several thalamic and hypothalamic nuclei, including periventricular nucleus of posterior tuberculum, lateral tuberal nucleus (NLT), and nucleus of the lateral recess (NRL). Scattered tac3-expressing cells are also present in telencephalic parts, such as ventral (Vv) and supracomissural (Vs) part of ventral telencephalon. In contrast to other teleosts, tac3 expression was absent from the pituitary. Using double-fluorescent staining, we localized tac3a-expressing cells in relation to GnRH and kisspeptin cells. Although no GnRH-tac3a colabeled cells were observed, dense GnRH fibers surround and potentially synapse with tac3a cells in the preoptic area. Only minimal (
Hans A. Hofmann - One of the best experts on this subject based on the ideXlab platform.
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Equal performance but distinct behaviors: Astatotilapia Burtoni sex differences in a novel object recognition task and spatial maze
2020Co-Authors: Kelly J Wallace, Hans A. HofmannAbstract:Sex differences in behavior and cognition can be driven by differential selection pressures from the environment and in the underlying neuromolecular mechanisms of decision-making. The highly social cichlid fish Astatotilapia Burtoni exhibits dynamic and complex social hierarchies, yet explicit cognitive testing (outside of social contexts) and investigations of sex differences in cognition have yet to be fully explored. Here we assessed male and female A. Burtoni in two cognitive tasks: a novel object recognition task and a spatial task. We hypothesized that given both males and females navigate dynamic social environments, we would observe less pronounced sex differences in cognition relative to other species with more "static" sex differences. In the present study we find that both sexes prefer the familiar object in a novel object recognition task, but the time at which they exhibit this preference differs between the sexes. Females more frequently learned a spatial task, exhibiting longer decision latencies and quicker error correction, suggesting a potential speed-accuracy tradeoff. Furthermore, the sexes differ in space use in both tasks and in a principal component analysis of the spatial task. A model selection analysis finds that preference, approach, and interaction duration in the novel object recognition task that reach a threshold of importance averaged across all models. This work highlights the need to explicitly test for sex differences in cognition to better understand how individuals navigate dynamic social environments. Highlights- To ask if sexual dimorphism in cognition is reduced in a species where both sexes navigate highly fluctuating social environments, we assessed performance and behavior of the cichlid fish Astatotilapia Burtoni in a novel object recognition task and a spatial maze. - Both sexes exhibited a preference for the familiar object during a novel object recognition task, with males exhibiting the preference early in the task, whereas females exhibiting the preference late in the task. - In the spatial task, females reached the learning criterion more often than expected by chance, whereas males do not. Females exhibited significantly longer decision latencies and quicker error correction in the spatial task, suggesting a sex-specific speed-accuracy tradeoff. - The sexes differ in behaviors related to neophobia and decision latencies. - A model selection analysis to predict sex finds that novel object recognition task preference, approach, and interaction duration are the most important terms on average.
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Neuromolecular correlates of cooperation and conflict during territory defense in a cichlid fish.
Hormones and behavior, 2017Co-Authors: Chelsea A. Weitekamp, Hans A. HofmannAbstract:Cooperative behavior is widespread among animals, yet the neural mechanisms have not been studied in detail. We examined cooperative territory defense behavior and associated neural activity in candidate forebrain regions in the cichlid fish, Astatotilapia Burtoni. We find that a territorial male neighbor will engage in territory defense dependent on the perceived threat of the intruder. The resident male, on the other hand, engages in defense based on the size and behavior of his partner, the neighbor. In the neighbor, we find that an index of engagement correlates with neural activity in the putative homolog of the mammalian basolateral amygdala and in the preoptic area, as well as in preoptic dopaminergic neurons. In the resident, neighbor behavior is correlated with neural activity in the homolog of the mammalian hippocampus. Overall, we find distinct neural activity patterns between the neighbor and the resident, suggesting that an individual perceives and processes an intruder challenge differently during cooperative territory defense depending on its own behavioral role.
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Arginine vasotocin regulates social ascent in the African cichlid fish Astatotilapia Burtoni.
General and comparative endocrinology, 2014Co-Authors: Lin S. Huffman, Flora I. Hinz, Sophie Wojcik, Nadia Aubin-horth, Hans A. HofmannAbstract:Neuropeptides modulate many aspects of behavior and physiology in a broad range of animals. Arginine vasotocin (AVT) is implicated in mediating social behavior in teleost fish, although its specific role varies between species, sexes, life stages, and social context. To investigate whether the effects of AVT on behavior depend on social context, we used the African cichlid fish Astatotilapia Burtoni, which is well-known for its remarkable behavioral plasticity. We pharmacologically manipulated the AVT system in established socially dominant and subordinate A. Burtoni males, as well as in males ascending to dominance status in a socially unstable environment. Our results show that exogenous AVT causes a stress response, as evidenced by reduced behavioral activity and increased circulating levels of cortisol in established dominant and subordinate males. Administration of the AVT antagonist Manning compound, on the other hand, did not affect established subordinate or dominant males. However, AVT antagonist-treated males ascending from subordinate to dominant status exhibited reduced aggressive and increased courtship behavior compared to vehicle-treated animals. Finally, we measured circulating cortisol levels and brain gene expression levels of AVT and its behaviorally relevant V1a2 receptor in all three social phenotypes and found that plasma cortisol and mRNA levels of both genes were increased in ascending males compared to dominant and subordinate males. Our results provide a more detailed understanding of the role of the AVT system in the regulation of complex behavior in a dynamically changing social environment.
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Aromatase regulates aggression in the African cichlid fish Astatotilapia Burtoni.
Physiology & Behavior, 2013Co-Authors: Lin S. Huffman, Lauren A. O’connell, Hans A. HofmannAbstract:The roles of estrogen and androgens in male social behavior are well studied, but little is known about how these hormones contribute to behavior in a social hierarchy. Here we test the role of aromatase, the enzyme that converts testosterone into estradiol, in mediating aggression and reproductive behavior in male Astatotilapia Burtoni, an African cichlid fish that displays remarkable plasticity in social behavior. We first measured aromatase expression in subordinate and dominant males in brain regions that regulate social behavior and found that subordinate males have higher aromatase expression than dominant males in the magnocellular and gigantocellular regions of the preoptic area. Next, we functionally tested the role of aromatase in regulating behavior by intraperitoneally injecting dominant males with either saline or fadrozole (FAD), an aromatase inhibitor, and found that FAD treatment decreases aggressive, but not reproductive, behaviors compared to saline controls. To determine the underlying physiological and molecular consequences of FAD treatment, we measured estradiol and testosterone levels from plasma and brain aromatase expression in FAD and saline treated dominant males. We found that estradiol levels decreased and testosterone levels increased in response to FAD treatment. Moreover, FAD treated males had increased aromatase expression in the gigantocellular portion of the POA, possibly a compensatory response. Overall, our results suggest aromatase is a key enzyme that promotes aggression in A. Burtoni males through actions in the preoptic area.
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Neurochemical profiling of dopaminergic neurons in the forebrain of a cichlid fish, Astatotilapia Burtoni.
Journal of chemical neuroanatomy, 2013Co-Authors: Lauren A. O’connell, Miles R. Fontenot, Hans A. HofmannAbstract:Across vertebrates, the mesolimbic reward system is a highly conserved neural network that serves to evaluate the salience of environmental stimuli, with dopamine as the neurotransmitter most relevant to its function. Although brain regions in the dopaminergic reward system have been well characterized in mammals, homologizing these brain areas with structures in teleosts has been controversial, especially for the mesencephalo-diencephalic dopaminergic cell populations. Here we examine the neurochemical profile of five dopaminergic cell groups (Vc, POA, PPr, TPp, pTn) in the model cichlid Astatotilapia Burtoni to better understand putative homology relationships between teleosts and mammals. We characterized in the adult brain the expression patterns of three genes (etv5, nr4a2, and pitx3) that either specify dopaminergic cell fate or maintain dopaminergic cell populations. We then determined whether these genes are expressed in dopaminergic cells. We find many striking similarities in these gene expression profiles between dopaminergic cell populations in teleosts and their putative mammalian homologs. Our results suggest that many of these dopaminergic cell groups are indeed evolutionarily ancient and conserved across vertebrates.
Thomas G. Preuss - One of the best experts on this subject based on the ideXlab platform.
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Social context influences sensorimotor gating in female African cichlid fish Astatotilapia Burtoni.
Behavioural brain research, 2019Co-Authors: Mila Adelman, H. Neumeister, Ai Ying Chen, Audrey Aberg, Thomas G. PreussAbstract:Abstract Disruption in prepulse inhibition (PPI), a sensorimotor gating phenomenon found in many species, has been associated with various psychiatric disorders in humans. Social defeat has been identified as a mediator of naturally evoked reductions of PPI in African cichlid fish Astatotilapia Burtoni where males reversibly alter social status and their sensorimotor gating abilities. Here we investigated A. Burtoni females, which establish a male-like social hierarchy with dominant (DOM) and subordinate (SUB) individuals when housed in communities without males. We asked if DOM and SUB females demonstrate socially induced PPI differences comparable to their male DOM and SUB counterparts. Results suggest that social defeat reduced PPI in SUB females as compared to DOM females (p = 0.033) and mixed-sex community female controls (p = 0.017). However, socially defeated females in same-sex communities remained proactive when engaging in antagonistic behaviors, which appears beneficial in avoiding substantial reductions in PPI as seen in reactive, socially defeated males. In open field swimming tests, SUB females exhibited increased anxiety-related behavior (thigmotaxis) as compared to females from mixed-sex communities (COM). Taken together, our results emphasize social defeat is a reliable modulator of PPI independent of sex, and anxiety related to social defeat might be a factor in mediating PPI plasticity.
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Socially induced plasticity in sensorimotor gating in the African cichlid fish Astatotilapia Burtoni
Behavioural brain research, 2017Co-Authors: H. Neumeister, Mila Adelman, William Gallagher, Jiangtao Gou, Karin Merrins, Melissa Perkowski, Stephanie Shih, Beth Terranova, Thomas G. PreussAbstract:Abstract Deficits in prepulse inhibition (PPI), social defeat and social withdrawal are hallmark features of several neurological and neuropsychiatric disorders. However, the link between social environment and PPI i.e., the possible role of social defeat in driving PPI plasticity, is far from clear. Here we explored these questions in the African cichlid fish Astatotilapia Burtoni , where males exist as two distinct yet reversible phenotypes. In fish communities, DOMs exhibit frequent aggressive and territorial behaviors, threatening and attacking SUBs, which respond either by engaging in fights and fleeing, or by avoiding interaction with DOMs altogether. Social phenotypes were selected using focal observations of dominant and submissive behaviors. Tests of auditory PPI showed markedly decreased PPI in SUBs as compared to DOMs at prepulse/pulse interstimulus interval of ISI 50 ms. Interestingly, further analysis showed the PPI reduction in SUBs was driven by males with low social interactivity. Testing males before and after social transitions revealed increasing and decreasing PPI in ascending and descending males, respectively. In an open field paradigm, SUBs also showed higher levels of wall hugging (thigmotaxis) and freezing when compared to DOMs i.e., an increase in anxiety-related behavior. Together the results suggest distinct yet reversible behavioral PPI phenotypes in A. Burtoni males, and that social defeat drives PPI plasticity. The fact that PPI deficits are readily reversible by status change implies PPI plasticity may reflect an adaptive response to challenges in the social environment.
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Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit.
Journal of neurophysiology, 2011Co-Authors: Keith W. Whitaker, H. Neumeister, Lin S. Huffman, Thomas G. Preuss, Celeste E. Kidd, Hans A. HofmannAbstract:Social life affects brain function at all levels, including gene expression, neurochemical balance, and neural circuits. We have previously shown that in the cichlid fish Astatotilapia Burtoni brig...
