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1. Behavioural tactic predicts preoptic-hypothalamic gene expression more strongly than developmental morph in fish with alternative reproductive tactics

   https://doi.org/10.1098/rspb.2017.2742  

   Tripp, Joel A. ; Feng, Ni Y. ; Bass, Andrew H. ( January 2018 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Reproductive success relies on the coordination of social behaviours, such as territory defence, courtship and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behaviour plasticity. The plainfin midshipman ( Porichthys notatus ) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioural tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioural tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behaviour. Our results reveal that divergent expression patterns in a conserved neuroendocrine centre known to regulate social-reproductive behaviours across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics. 

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2. Reproductive state modulates utricular auditory sensitivity in a vocal fish

   https://doi.org/10.1152/jn.00315.2022  

   Rogers, Loranzie S. ; Coffin, Allison B. ; Sisneros, Joseph A. ( November 2022 , Journal of Neurophysiology)

   The plainfin midshipman, Porichthys notatus, is a seasonally breeding vocal fish that relies on acoustic communication to mediate nocturnal reproductive behaviors. Reproductive females use their auditory senses to detect and localize “singing” males that produce multiharmonic advertisement (mate) calls during the breeding season. Previous work showed that the midshipman saccule, which is considered the primary end organ used for hearing in midshipman and most other fishes, exhibits reproductive state and hormone-dependent changes that enhance saccular auditory sensitivity. In contrast, the utricle was previously posited to serve primarily a vestibular function, but recent evidence in midshipman and related toadfish suggests that it may also serve an auditory function and aid in the detection of behaviorally relevant acoustic stimuli. Here, we characterized the auditory-evoked potentials recorded from utricular hair cells in reproductive and nonreproductive female midshipman in response to underwater sound to test the hypothesis that variation in reproductive state affects utricular auditory sensitivity. We show that utricular hair cells in reproductive females exhibit up to a sixfold increase in the utricular potential magnitude and have thresholds based on measures of particle acceleration (re: 1 ms −2 ) that are 7–10 dB lower than nonreproductive females across a broad range of frequencies, which include the dominant harmonics of male advertisement calls. This enhanced auditory sensitivity of the utricle likely plays an essential role in facilitating midshipman social and reproductive acoustic communication. NEW & NOTEWORTHY In many animals, vocal-acoustic communication is fundamental for facilitating social behaviors. For the vocal plainfin midshipman fish, the detection and localization of social acoustic signals are critical to the species’ reproductive success. Here, we show that the utricle, an inner ear end organ often thought to primarily serve a vestibular function, serves an auditory function that is seasonally plastic and modulated by the animal’s reproductive state effectively enhancing auditory sensitivity to courting male advertisement calls. 

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3. Melatonin receptor expression in vocal, auditory, and neuroendocrine centers of a highly vocal fish, the plainfin midshipman ( Porichthys notatus )

   https://doi.org/10.1002/cne.24629  

   Feng, Ni Y. ; Marchaterre, Margaret A. ; Bass, Andrew H. ( January 2019 , Journal of Comparative Neurology)

   Melatonin plays a central role in entraining activity to the day–night cycle in vertebrates. Here, we investigate neuroanatomical substrates of melatonin‐dependent vocal–acoustic behavior in the nocturnal and highly vocal teleost fish, the plainfin midshipman (Porichthys notatus). Using in situ hybridization (ISH) and quantitative real‐time PCR (qPCR), we assess the mRNA distribution and transcript abundance of melatonin receptor subtype 1B (mel1b), shown to be important for vocalization in midshipman fish and songbirds. ISH shows robustmel1bexpression in major nodes of the central vocal and auditory networks in the subpallium, preoptic area (POA), anterior hypothalamus, dorsal thalamus, posterior tuberculum, midbrain torus semicircularis and periaqueductal gray, and hindbrain.Mel1blabel is also abundant in secondary targets of the olfactory, visual, and lateral line systems, as well as telencephalic regions that have been compared to the amygdala, extended amygdala, striatum, septum, and hippocampus of tetrapods. Q‐PCR corroboratesmel1babundance throughout the brain and shows significant increases in the morning compared with nighttime in tissue samples inclusive of the telencephalon and POA, but remains stable in other brain regions. Plasma melatonin levels show expected increase at night. Our findings support the hypothesis that melatonin's stimulatory effects on vocal–acoustic mechanisms in midshipman is mediated, in part, by melatonin binding in vocal, auditory, and neuroendocrine centers. Together with robustmel1bexpression in multiple telencephalic nuclei and sensory systems, the results further indicate an expression pattern comparable to that in birds and mammals that is indicative of melatonin's broad involvement in the modulation of physiology and behavior.

    

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

   https://doi.org/10.1002/cne.25383  

   Mobley, Robert B. ; Ray, Emily J. ; Maruska, Karen P. ( July 2022 , Journal of Comparative Neurology)

   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 ofnnos‐expressing cells in the brain and retina of the cichlid fishAstatotilapia burtoniusing 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 innnosexpression within the eye and olfactory bulbs of males and females of different reproductive states and social statuses. In the eye, males express morennosthan females, and socially dominant males express morennosthan subordinate males, but expression did not differ among female reproductive states. In the olfactory bulbs, dominant males had greaternnosexpression 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 ofnnos‐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.

    

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5. Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour, sperm characteristics and social interactions

   https://doi.org/10.1111/mec.14999  

   Nugent, Bridget M. ; Stiver, Kelly A. ; Hofmann, Hans A. ; Alonzo, Suzanne H. ( February 2019 , Molecular Ecology)

   While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.

    

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