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  • Opsin expression varies with reproductive state in the cichlid fish Astatotilapia burtoni. Integrative and comparative biology Butler, J. M., Maruska, K. P. 2021


    Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared to non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared to mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.

    View details for DOI 10.1093/icb/icab058

    View details for PubMedID 33972997

  • Reproductive- and social-state plasticity of multiple sensory systems in a cichlid fish. Integrative and comparative biology Maruska, K. P., Butler, J. M. 2021


    Intra- and inter-sexual communication is 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 function 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, biogenic amines) occurs at both peripheral sensory organs (eye, inner ear, 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.

    View details for DOI 10.1093/icb/icab062

    View details for PubMedID 33963407

  • Expression patterns and evolution of urocortin and corticotropin-releasing hormone genes in a cichlid fish. The Journal of comparative neurology Grone, B. P., Butler, J. M., Wayne, C. R., Maruska, K. P. 2021


    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.

    View details for DOI 10.1002/cne.25113

    View details for PubMedID 33474732

  • Galanin neuron activation in feeding, parental care, and infanticide in a mouthbrooding African cichlid fish. Hormones and behavior Butler, J. M., Herath, E. M., Rimal, A., Whitlow, S. M., Maruska, K. P. 2020: 104870


    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.

    View details for DOI 10.1016/j.yhbeh.2020.104870

    View details for PubMedID 33002455

  • Female reproductive state is associated with changes in distinct arginine vasotocin cell types in the preoptic area ofAstatotilapia burtoni JOURNAL OF COMPARATIVE NEUROLOGY Butler, J. M., Anselmo, C. M., Maruska, K. P. 2020


    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.

    View details for DOI 10.1002/cne.24995

    View details for Web of Science ID 000563985600001

    View details for PubMedID 32706120

  • 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 Butler, J. M., Maruska, K. P. 2020


    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 ~2weeks 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-hr period of excess noise (~140dB) 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 to control broods. Further, onset of adult-typical coloration and behaviors was delayed compared to 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.

    View details for DOI 10.1111/gbb.12692

    View details for PubMedID 32779314

  • Neural activation patterns associated with maternal mouthbrooding and energetic state in an African cichlid fish. Neuroscience Maruska, K. P., Butler, J. M., Field, K. E., Forester, C., Augustus, A. 2020


    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.

    View details for DOI 10.1016/j.neuroscience.2020.07.025

    View details for PubMedID 32707292

  • Underwater noise impairs social communication during aggressive and reproductive encounters ANIMAL BEHAVIOUR Butler, J. M., Maruska, K. P. 2020; 164: 9–23