Cichlid Fish Astatotilapia Burtoni Research Articles

Multiple behavioral mechanisms shape development in a highly social cichlid fish

Early-life social experiences shape adult phenotype, yet the underlying behavioral mechanisms remain poorly understood. We manipulated early-life social experience in the highly social African cichlid fish Astatotilapia burtoni to investigate the effects on behavior and stress axis function in juveniles. Juveniles experienced different numbers of social partners in stable pairs (1 partner), stable groups (6 fish; 5 partners), and socialized pairs (a novel fish was exchanged every 5 days; 5 partners). Treatments also differed in group size (groups vs. pairs) and stability (stable vs. socialized). We then measured individual behavior and water-borne cortisol to identify effects of early-life experience. We found treatment differences in behavior across all assays: open field exploration, social cue investigation, dominant behavior, and subordinate behavior. Treatment did not affect cortisol. Principal components (PC) analysis revealed robust co-variation of behavior across contexts, including with cortisol, to form behavioral syndromes sensitive to early-life social experience. PC1 (25.1 %) differed by social partner number: juveniles with more partners (groups and socialized pairs) were more exploratory during the social cue investigation, spent less time in the territory, and were more interactive as dominants. PC5 (8.5 %) differed by stability: socialized pairs were more dominant, spent less time in and around the territory, were more socially investigative, and had lower cortisol than stable groups or pairs. Observations of the home tanks provided insights into the social experiences that may underlie these effects. These results contribute to our understanding of how early-life social experiences are accrued and exert strong, lasting effects on phenotype.

Neural activation patterns associated with mouthbrooding, maternal care, infanticide and fry release in an African cichlid fish.

Parental care has evolved several times and is present across taxa. Parental care behaviors, such as food provisioning and protection, are critical for offspring success. However, infanticide can co-exist with parental care in the same species. The mechanisms underlying the switch from care to consumption and from offspring dependence to independence are relatively unknown, especially in fishes, the oldest and largest group of vertebrates. Mouthbrooding, an extreme example of parental care present in dozens of genera of fishes, provides an excellent opportunity to investigate the brain regions important for parental care. The maternal mouthbrooding African cichlid fish Astatotilapia burtoni broods developing young inside the mouth for approximately 14 days, then provides post-release maternal care by protecting fry inside the mouth when threatened. Following the post-release maternal care phase, females can exhibit infanticide and consume their own offspring. We used immunohistochemistry for the neural activation marker pS6 to identify differences in neural activation among mouthbrooding, maternal-care-providing and infanticide-exhibiting females, and between pre- and post-release fry. We identified five brain regions (Dc-5, ATn, nPPa, Vd-c and Dl-g) that are differentially activated among mouthbrooding, maternal care and infanticide females as well as six regions (Dm, Vv, Vd, Vs-m, TPp, PGZ and INL of retina) differentially activated between pre- and post-release fry. This study identifies both shared and distinct circuitry that may support transitions between parental care states and from care to infanticide, as well as regions in developed fry that support the transition from pre- to post-release.

Expression and localization of neuronal nitric oxide synthase in the brain and sensory tissues of the African cichlid fish Astatotilapia burtoni.

Nitric oxide (NO) produced by the enzyme neuronal nitric oxide synthase serves as an important neurotransmitter in the central nervous system that is involved in reproductive regulation, learning, sensory processing, and other forms of neural plasticity. Here, we map the distribution of nnos-expressing cells in the brain and retina of the cichlid fish Astatotilapia burtoni using in situ hybridization. In the brain, nnos-expressing cells are found from the olfactory bulbs to the hindbrain, including within specific nuclei involved in decision-making, sensory processing, neuroendocrine regulation, and the expression of social behaviors. In the retina, nnos-expressing cells are found in the inner nuclear layer, presumably in amacrine cells. We also used quantitative PCR to test for differences in nnos expression within the eye and olfactory bulbs of males and females of different reproductive states and social statuses. In the eye, males express more nnos than females, and socially dominant males express more nnos than subordinate males, but expression did not differ among female reproductive states. In the olfactory bulbs, dominant males had greater nnos expression than subordinate males. These results suggest a status-specific function for NO signaling in the visual and olfactory systems that may be important for sensory perception related to mating or territorial interactions to maintain the social hierarchy. The widespread distribution of nnos-expressing cells throughout the cichlid brain is similar to that in other teleosts, with some conserved localization patterns across vertebrates, suggesting diverse functions for this important neurotransmitter system.

Doublecortin in the Fish Visual System, a Specific Protein of Maturing Neurons.

Simple SummaryDoublecortin (DCX) is an essential protein in the development of the central nervous system and in lamination of the mammalian cortex. It is known that the expression of DCX is restricted to newborn neurons. The visual system of teleost fish has been postulated as an ideal model since it continuously grows throughout the animal’s life. Here, we report a comparative expression analysis of DCX between two teleost fish species as well as a bioinformatic analysis with other animal groups. Our results demonstrate that DCX is very useful for identifying new neurons in the visual systems of Astatotilapia burtoni, but is absent in Danio rerio.Doublecortin (DCX) is a microtubule associated protein, essential for correct central nervous system development and lamination in the mammalian cortex. It has been demonstrated to be expressed in developing—but not in mature—neurons. The teleost visual system is an ideal model to study mechanisms of adult neurogenesis due to its continuous life-long growth. Here, we report immunohistochemical, in silico, and western blot analysis to detect the DCX protein in the visual system of teleost fish. We clearly determined the expression of DCX in newly generated cells in the retina of the cichlid fish Astatotilapia burtoni, but not in the cyprinid fish Danio rerio. Here, we show that DCX is not associated with migrating cells but could be related to axonal growth. This work brings to light the high conservation of DCX sequences between different evolutionary groups, which make it an ideal marker for maturing neurons in various species. The results from different techniques corroborate the absence of DCX expression in zebrafish. In A. burtoni, DCX is very useful for identifying new neurons in the transition zone of the retina. In addition, this marker can be applied to follow axons from maturing neurons through the neural fiber layer, optic nerve head, and optic nerve.

Social instability influences rank-specific patterns of oxidative stress in a cichlid fish.

In many animal societies, dominant individuals have priority access to resources. However, defending high rank can be costly, especially in unstable social hierarchies where there is more intense competition. Oxidative stress has been proposed as a potential cost of social dominance, but few studies have examined this cost in relation to social stability. We studied the cost of social dominance in the cichlid fish Astatotilapia burtoni by manipulating social stability among males in replicate naturalistic communities for 22 weeks. We found that our social stability treatment influenced status-specific patterns in 3 out of 6 measurements of oxidative stress. Specifically, dominant males experienced increased plasma oxidative damage (measured as reactive oxygen metabolites, ROMs) compared with subordinate males in stable hierarchies only. Subordinate males in unstable hierarchies had higher ROMs than their stable community counterparts, but we found no effect of social stability treatment for dominant males. However, dominant males tended to have reduced total antioxidant capacity (TAC) in the liver when compared with subordinate males in unstable hierarchies, suggesting that the cost of social dominance is higher in unstable hierarchies. There were no effects of status and treatment on gonad TAC, muscle TAC or oxidative DNA damage. We conclude that the stability of the social environment influences the relative cost of social dominance in a tissue- and marker-specific manner.

Opsin Expression Varies with Reproductive State in the Cichlid Fish Astatotilapia burtoni.

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 with 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 with 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.

Spiny and soft-rayed fin domains in acanthomorph fish are established through a BMP-gremlin-shh signaling network

With over 18,000 species, the Acanthomorpha, or spiny-rayed fishes, form the largest and arguably most diverse radiation of vertebrates. One of the key novelties that contributed to their evolutionary success are the spiny rays in their fins that serve as a defense mechanism. We investigated the patterning mechanisms underlying the differentiation of median fin Anlagen into discrete spiny and soft-rayed domains during the ontogeny of the direct-developing cichlid fish Astatotilapia burtoni Distinct transcription factor signatures characterize these two fin domains, whereby mutually exclusive expression of hoxa13a/b with alx4a/b and tbx2b marks the spine to soft-ray boundary. The soft-ray domain is established by BMP inhibition via gremlin1b, which synergizes in the posterior fin with shh secreted from a zone of polarizing activity. Modulation of BMP signaling by chemical inhibition or gremlin1b CRISPR/Cas9 knockout induces homeotic transformations of spines into soft rays and vice versa. The expression of spine and soft-ray genes in nonacanthomorph fins indicates that a combination of exaptation and posterior expansion of an ancestral developmental program for the anterior fin margin allowed the evolution of robustly individuated spiny and soft-rayed domains. We propose that a repeated exaptation of such pattern might underly the convergent evolution of anterior spiny-fin elements across fishes.

A behavioral logic underlying aggression in an African cichlid fish

AbstractSocial 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 behaviors underlying responses to males of different sizes are not well understood. In many other fish species, when size asymmetries between competing males are small, physical aggression is likely to be used to settle territorial disputes. Our goal was to characterize these responses in male A. burtoni 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 that were smaller than the intruder (resident >5% smaller in SL) or matched (resident between 0 and 5% smaller or larger in SL) in size to the intruder performed more lateral displays, a type of non‐physical aggression, than resident males that were larger than the intruder (resident >5% larger in SL). However, physical aggression, such as chases and bites, did not differ as a function of relative SL. Thus, contrary to what was expected based on work in other species, our results demonstrate that dominant resident A. burtoni increase non‐physical aggression to settle territorial disputes when non‐dominant intruders are closer in size. This behavioral strategy may aid in readily settling conflicts when size asymmetries are small.

Reproductive- and Social-State Plasticity of Multiple Sensory Systems in a Cichlid Fish.

Intra- and inter-sexual communications are vital to the survival and reproductive success of animals. In species that cycle in and out of breeding or other physiological condition, sensory function can be modulated to optimize communication at crucial times. Little is known, however, about how widespread this sensory plasticity is across taxa, whether it occurs in multiple senses or both sexes within a species, and what potential modulatory substances and substrates are involved. Thus, studying modulation of sensory communication in a single species can provide valuable insights for understanding how sensory abilities can be altered to optimize detection of salient signals in different sensory channels and social contexts. The African cichlid fish Astatotilapia burtoni uses multimodal communication in social contexts such as courtship, territoriality, and parental care and shows plasticity in sensory abilities. In this review, we synthesize what is known about how visual, acoustic, and chemosensory communication is used in A. burtoni in inter- and intra-specific social contexts, how sensory funtion is modulated by an individual's reproductive, metabolic, and social state, and discuss evidence for plasticity in potential modulators that may contribute to changes in sensory abilities and behaviors. Sensory plasticity in females is primarily associated with the natural reproductive cycle and functions to improve detection of courtship signals (visual, auditory, chemosensory, and likely mechanosensory) from high-quality males for reproduction. Plasticity in male sensory abilities seems to function in altering their ability to detect the status of other males in the service of territory ownership and future reproductive opportunities. Changes in different classes of potential modulators or their receptors (steroids, neuropeptides, and biogenic amines) occur at both peripheral sensory organs (eye, inner ear, and olfactory epithelium) and central visual, olfactory, and auditory processing regions, suggesting complex mechanisms contributing to plasticity of sensory function. This type of sensory plasticity revealed in males and females of A. burtoni is likely more widespread among diverse animals than currently realized, and future studies should take an integrative and comparative approach to better understand the proximate and ultimate mechanisms modulating communication abilities across taxa.

Equal performance but distinct behaviors: sex differences in a novel object recognition task and spatial maze in a highly social cichlid fish.

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 males outperform females in a spatial learning task and exhibit more neophilic/exploratory behavior across both tasks. 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 the 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 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.

Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni.

In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens. These animals grow to a standard length of 10-12 cm in this fish species, corresponding to a more than 100-fold increase in brain volume. Focusing on the telencephalon where glial cells are arranged radially in the everted (dorsal) pallium, immunocytochemistry for glial markers revealed an aberrant pattern of radial glial fibers in the central division of the dorsal pallium (DC, i.e., DC4 and DC5). The main glial processes curved around these nuclei, especially in the posterior part of the telencephalon. This was verified in tissue-cleared brains stained for glial markers. We further analyzed the growth of radial glia by immunocytochemically applied stem cell (proliferating cell nuclear antigen [PCNA], Sox2) and differentiation marker (doublecortin) and found that these markers were expressed at the ventricular surface consistent with a stacking growth pattern. In addition, we detected doublecortin and Sox2 positive cells in deeper nuclei of DC areas. Our data suggest that radial glial cells give rise to migrating cells providing new neurons and glia to deeper pallial regions. This results in expansion of the central pallial areas and displacement of existing radial glial. In summary, we show that radial glial cells can adapt to morphological growth processes in the adult fish brain and contribute to this growth.

Expression patterns and evolution of urocortin and corticotropin-releasing hormone genes in a cichlid fish.

The corticotropin-releasing hormone and urocortin family of peptides consists of five members in many vertebrates: CRH (crha/crhb in teleosts), CRH2, UCN/UTS1, UCN2, and UCN3. These genes differ in expression pattern, as well as receptor affinity, allowing them to serve a wide range of functions in a variety of species. To better understand the roles of these genes in a single species, we examined their expression patterns in the cichlid fish Astatotilapia burtoni. In situ hybridization to map mRNA expression patterns of crhb, uts1, ucn2, and ucn3 in the brain revealed conserved and distinct spatial features of expression. crhb- and uts1-expressing cells were the most broadly distributed, with several areas of co-regionalization. ucn3 was less abundant but was found in discrete regions throughout the extent of the brain, with high expression in the cerebellum, while ucn2 was restricted to only a few areas. RT-PCR showed that while crhb, uts1, and ucn3 are found in several body tissues and widespread throughout the brain, ucn2 is quite restricted in the brain, and crha is only expressed in the eye. Bayesian phylogenetic analyses identified detailed relationships and novel orthologs in the urocortin family. We found evidence for a UCN2 gene loss in some reptiles. Our detailed description of the complete family of genes in the central nervous system of a model organism will inform future studies on the function of these genes in A. burtoni and provides a foundation for comparative studies with teleosts and other vertebrates.

Radical change: temporal patterns of oxidative stress during social ascent in a dominance hierarchy

Dominant individuals have priority access to mates and resources. However, high rank can be costly too, especially when it is maintained by intense agonistic behavior. Oxidative stress has been proposed as a potential cost of social dominance. However, social dominance hierarchies can be dynamic, and few studies have examined the cost of social dominance when males are changing status. We studied temporal changes in markers of oxidative stress during social ascent in the East African cichlid fish Astatotilapia burtoni. After removing the dominant male, males ascended from subordinate to dominant status. On the first day of social ascent, immediately after the dominant male removal, the newly dominant male showed lower levels of plasma total antioxidant capacity (TAC). However, we found that liver TAC and liver superoxide dismutase (SOD), an enzymatic antioxidant, were significantly upregulated on day 1 and 2 of social ascent, respectively. No temporal variation in nicotinamide adenine dinucleotide phosphate-oxidase (NADPH-oxidase) activity, blood DNA damage, and liver DNA damage was observed. By day 14, all markers of oxidative stress were similar to those observed in stable dominant males, which had higher levels of reactive oxygen metabolites (ROM) compared to subordinate males. We conclude that markers of oxidative stress vary dramatically during social ascent in a time- and tissue-dependent manner. Our study provides a more nuanced look at the oxidative cost of social dominance and highlights the importance of considering temporal changes in markers of oxidative stress during important life-history events. High social status gives priority access to resources but also entails costs. Since dominant individuals tend to have higher metabolic rates, oxidative stress could be a potential cost of high social status. Oxidative stress can occur when reactive oxygen species, produced during metabolic activities, cannot be effectively neutralized by antioxidants, leading to oxidative cellular damage. Social hierarchies can be dynamic, yet how the cost of rank varies when males are changing social status is unknown. We allowed subordinate males to ascend to dominant status in the cichlid fish Astatotilapia burtoni. At the beginning of social ascent when males suddenly increase aggressive behavior, the total antioxidant defense was lower in blood plasma, as expected, when males suddenly increase their metabolism during aggressive interactions. However, antioxidant defense was increased in the liver suggesting that males can compensate for the potential cost of becoming dominant. Circulating reactive oxygen metabolites gradually increased over time reaching levels similar to stable dominant males, possibly due to males upregulating their reproductive axis. Our results highlight that markers of oxidative stress can vary dramatically over time during important events in life.

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish.

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild-caught individuals. Here, we investigated the contribution of habitat-specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake-river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake-like pond set-up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set-up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set-up were based on a plastic response. Finally, gene expression and bacterial communities of wild-caught individuals and individuals acclimatized to lake-like pond conditions showed shifts underlying adaptive phenotypic plasticity.

Galanin neuron activation in feeding, parental care, and infanticide in a mouthbrooding African cichlid fish

Galanin is a conserved neuropeptide involved in parental care and feeding. While galanin is known to mediate parental care and infanticide in rodents, its role in parental care and feeding behaviors in other taxa, particularly fishes, remains poorly understood. Mouthbrooding is an extreme form of parental care common in fishes in which caregivers carry offspring in their buccal cavity for the duration of development, resulting in obligatory starvation. In the cichlid fish Astatotilapia burtoni, females brood their young for ~2 wks and perform maternal care after release by collecting them into their mouth when threatened. However, females will cannibalize their brood after ~5 days. To examine the role of gal in feeding and maternal care, we collected mouthbrooding, fed, and starved females, as well as those displaying post-release maternal care and infanticide behaviors. Activation of gal neurons in the preoptic area (POA) was associated with parental care, providing the first link between gal and offspring-promoting behaviors in fishes. In contrast, activation of gal neurons in the lateral tuberal nucleus (NLT), the Arcuate homolog, was associated with feeding and infanticide. Overall, these data suggest gal is functionally conserved across vertebrate taxa with POA gal neurons promoting maternal care and Arc/NLT gal neurons promoting feeding.

Neural Activation Patterns Associated with Maternal Mouthbrooding and Energetic State in an African Cichlid Fish

Parental care is widespread in the animal kingdom, but for many species, provisioning energetic resources must be balanced with trade-offs between self-promoting and offspring-promoting behaviors. However, little is known about the neural mechanisms underlying these motivational decisions. Mouthbrooding is an extreme form of parental care most common in fishes that provides an ideal opportunity to examine which brain regions are involved in parenting and energetics. The African cichlid fish Astatotilapia burtoni is a maternal mouthbrooder in which females hold developing young inside their mouths for 2 weeks. This brood care makes feeding impossible, so females undergo obligatory starvation. We used immunohistochemistry for the neural activation marker pS6 to examine which brain regions were involved in processing salient information in mouthbrooding, starved, and fed females. We identified brain regions more associated with maternal brood care (TPp, Dc-4/-5), and others reflective of energetic state (Dl-v, NLTi). Most nuclei examined, however, were involved in both maternal care and energetic status. Placement of each of the 16 examined nuclei into these functional categories was supported by node by node comparisons, co-activity networks, hierarchical clustering, and discriminant function analysis. These results reveal which brain regions are involved in parental care and food intake in a species where provisioning is skewed towards the offspring when parental feeding is not possible. This study provides support for both distinct and shared circuitry involved in regulation of maternal care, food intake, and energy balance, and helps put the extreme parental case of mouthbrooding into a comparative and evolutionary context.

Behavioral traits that define social dominance are the same that reduce social influence in a consensus task

Dominant individuals are often most influential in their social groups, affecting movement, opinion, and performance across species and contexts. Yet, behavioral traits like aggression, intimidation, and coercion, which are associated with and in many cases define dominance, can be socially aversive. The traits that make dominant individuals influential in one context may therefore reduce their influence in other contexts. Here, we examine this association between dominance and influence using the cichlid fish Astatotilapia burtoni, comparing the influence of dominant and subordinate males during normal social interactions and in a more complex group consensus association task. We find that phenotypically dominant males are aggressive, socially central, and that these males have a strong influence over normal group movement, whereas subordinate males are passive, socially peripheral, and have little influence over normal movement. However, subordinate males have the greatest influence in generating group consensus during the association task. Dominant males are spatially distant and have lower signal-to-noise ratios of informative behavior in the association task, potentially interfering with their ability to generate group consensus. In contrast, subordinate males are physically close to other group members, have a high signal-to-noise ratio of informative behavior, and equivalent visual connectedness to their group as dominant males. The behavioral traits that define effective social influence are thus highly context specific and can be dissociated with social dominance. Thus, processes of hierarchical ascension in which the most aggressive, competitive, or coercive individuals rise to positions of dominance may be counterproductive in contexts where group performance is prioritized.

Reproductive state-dependent plasticity in the visual system of an African cichlid fish

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.

Early-life social environment alters juvenile behavior and neuroendocrine function in a highly social cichlid fish

Early-life experiences can shape adult behavior, with consequences for fitness and health, yet fundamental questions remain unanswered about how early-life social experiences are translated into variation in brain and behavior. The African cichlid fish Astatotilapia burtoni, a model system in social neuroscience, is well known for its highly plastic social phenotypes in adulthood. Here, we rear juveniles in either social groups or pairs to investigate the effects of early-life social environments on behavior and neuroendocrine gene expression. We find that both juvenile behavior and neuroendocrine function are sensitive to early-life effects. Behavior robustly co-varies across multiple contexts (open field, social cue investigation, and dominance behavior assays) to form a behavioral syndrome, with pair-reared juveniles towards the end of syndrome that is less active and socially interactive. Pair-reared juveniles also submit more readily as subordinates. In a separate cohort, we measured whole brain expression of stress and sex hormone genes. Expression of glucocorticoid receptor 1a was elevated in group-reared juveniles, supporting a highly-conserved role for the stress axis mediating early-life effects. The effect of rearing environment on androgen receptor α and estrogen receptor α expression was mediated by treatment duration (1 vs. 5 weeks). Finally, expression of corticotropin-releasing factor and glucocorticoid receptor 2 decreased significantly over time. Rearing environment also caused striking differences in gene co-expression, such that expression was tightly integrated in pair-reared juveniles but not group-reared or isolates. Together, this research demonstrates the important developmental origins of behavioral phenotypes and identifies potential behavioral and neuroendocrine mechanisms.

Social context influences sensorimotor gating in female African cichlid fish Astatotilapia burtoni.

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.