skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: FoxP2 Expression in a Highly Vocal Teleost Fish with Comparisons to Tetrapods
Motivated by studies of speech deficits in humans, several studies over the past two decades have investigated the potential role of a forkhead domain transcription factor, FoxP2, in the central control of acoustic signaling/vocalization among vertebrates. Comparative neuroanatomical studies that mainly include mammalian and avian species have mapped the distribution of FoxP2 expression in multiple brain regions that imply a greater functional significance beyond vocalization that might be shared broadly across vertebrate lineages. To date, reports for teleost fish have been limited in number and scope to nonvocal species. Here, we map the neuroanatomical distribution of FoxP2 mRNA expression in a highly vocal teleost, the plainfin midshipman (Porichthys notatus). We report an extensive overlap between FoxP2 expression and vocal, auditory, and steroid-signaling systems with robust expression at multiple sites in the telencephalon, the preoptic area, the diencephalon, and the midbrain. Label was far more restricted in the hindbrain though robust in one region of the reticular formation. A comparison with other teleosts and tetrapods suggests an evolutionarily conserved FoxP2 phenotype important to vocal-acoustic and, more broadly, sensorimotor function among vertebrates.  more » « less
Award ID(s):
1457108
PAR ID:
10274986
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Brain, Behavior and Evolution
Volume:
91
Issue:
2
ISSN:
0006-8977
Page Range / eLocation ID:
82 to 96
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract 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. 
    more » « less
  2. Abstract Vocalization is a common means of communication across vertebrates, but the evolutionary origins of the neural circuits controlling these behaviors are not clear. Peripheral mechanisms of sound production vary widely: fish produce sounds with a swimbladder or pectoral fins; amphibians, reptiles, and mammalians vocalize using a larynx; birds vocalize with a syrinx. Despite the diversity of vocal effectors across taxa, there are many similarities in the neural circuits underlying the control of these organs. Do similarities in vocal circuit structure and function indicate that vocal behaviors first arose in a single common ancestor, or have similar neural circuits arisen independently multiple times during evolution? In this review, we describe the hindbrain circuits that are involved in vocal production across vertebrates. Given that vocalization depends on respiration in most tetrapods, it is not surprising that vocal and respiratory hindbrain circuits across distantly related species are anatomically intermingled and functionally linked. Such vocal‐respiratory circuit integration supports the hypothesis that vocal evolution involved the expansion and functional diversification of breathing circuits. Recent phylogenetic analyses, however, suggest vocal behaviors arose independently in all major tetrapod clades, indicating that similarities in vocal control circuits are the result of repeated co‐options of respiratory circuits in each lineage. It is currently unknown whether vocal circuits across taxa are made up of homologous neurons, or whether vocal neurons in each lineage arose from developmentally and evolutionarily distinct progenitors. Integrative comparative studies of vocal neurons across brain regions and taxa will be required to distinguish between these two scenarios. 
    more » « less
  3. Abstract The interface between field biology and technology is energizing the collection of vast quantities of environmental data. Passive acoustic monitoring, the use of unattended recording devices to capture environmental sound, is an example where technological advances have facilitated an influx of data that routinely exceeds the capacity for analysis. Computational advances, particularly the integration of machine learning approaches, will support data extraction efforts. However, the analysis and interpretation of these data will require parallel growth in conceptual and technical approaches for data analysis. Here, we use a large hand‐annotated dataset to showcase analysis approaches that will become increasingly useful as datasets grow and data extraction can be partially automated.We propose and demonstrate seven technical approaches for analyzing bioacoustic data. These include the following: (1) generating species lists and descriptions of vocal variation, (2) assessing how abiotic factors (e.g., rain and wind) impact vocalization rates, (3) testing for differences in community vocalization activity across sites and habitat types, (4) quantifying the phenology of vocal activity, (5) testing for spatiotemporal correlations in vocalizations within species, (6) among species, and (7) using rarefaction analysis to quantify diversity and optimize bioacoustic sampling.To demonstrate these approaches, we sampled in 2016 and 2018 and used hand annotations of 129,866 bird vocalizations from two forests in New Hampshire, USA, including sites in the Hubbard Brook Experiment Forest where bioacoustic data could be integrated with more than 50 years of observer‐based avian studies. Acoustic monitoring revealed differences in community patterns in vocalization activity between forests of different ages, as well as between nearby similar watersheds. Of numerous environmental variables that were evaluated, background noise was most clearly related to vocalization rates. The songbird community included one cluster of species where vocalization rates declined as ambient noise increased and another cluster where vocalization rates declined over the nesting season. In some common species, the number of vocalizations produced per day was correlated at scales of up to 15 km. Rarefaction analyses showed that adding sampling sites increased species detections more than adding sampling days.Although our analyses used hand‐annotated data, the methods will extend readily to large‐scale automated detection of vocalization events. Such data are likely to become increasingly available as autonomous recording units become more advanced, affordable, and power efficient. Passive acoustic monitoring with human or automated identification at the species level offers growing potential to complement observer‐based studies of avian ecology. 
    more » « less
  4. Abstract Galanin is a peptide that regulates pituitary hormone release, feeding, and reproductive and parental care behaviors. In teleost fish, increased galanin expression is associated with territorial, reproductively active males. Prior transcriptome studies of the plainfin midshipman (Porichthys notatus), a highly vocal teleost fish with two male morphs that follow alternative reproductive tactics, show that galanin is upregulated in the preoptic area‐anterior hypothalamus (POA‐AH) of nest‐holding, courting type I males during spawning compared to cuckolding type II males. Here, we investigate possible differences in galanin immunoreactivity in the brain of both male morphs and females with a focus on vocal‐acoustic and neuroendocrine networks. We find that females differ dramatically from both male morphs in the number of galanin‐expressing somata and in the distribution of fibers, especially in brainstem vocal‐acoustic nuclei and other sensory integration sites that also differ, though less extensively, between the male morphs. Double labeling shows that primarily separate populations of POA‐AH neurons express galanin and the nonapeptides arginine‐vasotocin or isotocin, homologues of mammalian arginine vasopressin and oxytocin that are broadly implicated in neural mechanisms of vertebrate social behavior including morph‐specific actions on vocal neurophysiology in midshipman. Finally, we report a small population of POA‐AH neurons that coexpress galanin and the neurotransmitter γ‐aminobutyric acid. Together, the results indicate that galanin neurons in midshipman fish likely modulate brain activity at a broad scale, including targeted effects on vocal motor, sensory and neuroendocrine systems; are unique from nonapeptide‐expressing populations; and play a role in male‐specific behaviors. 
    more » « less
  5. Abstract For many animal species, vocal communication is a critical social behavior and often a necessary component of reproductive success. Additionally, vocalizations are often demanding motor acts. Wanting to know whether a specific molecular toolkit might be required for vocalization, we used RNA‐sequencing to investigate neural gene expression underlying the performance of an extreme vocal behavior, the courtship hum of the plainfin midshipman fish (Porichthys notatus). Single hums can last up to 2 h and may be repeated throughout an evening of courtship activity. We asked whether vocal behavioral states are associated with specific gene expression signatures in key brain regions that regulate vocalization by comparing transcript expression levels in humming versus non‐humming males. We find that the circadian‐related genesperiod3andClockare significantly upregulated in the vocal motor nucleus and preoptic area‐anterior hypothalamus, respectively, in humming compared with non‐humming males, indicating that internal circadian clocks may differ between these divergent behavioral states. In addition, we identify suites of differentially expressed genes related to synaptic transmission, ion channels and transport, neuropeptide and hormone signaling, and metabolism and antioxidant activity that together may support the neural and energetic demands of humming behavior. Comparisons of transcript expression across regions stress regional differences in brain gene expression, while also showing coordinated gene regulation in the vocal motor circuit in preparation for courtship behavior. These results underscore the role of differential gene expression in shifts between behavioral states, in this case neuroendocrine, motor and circadian control of courtship vocalization. 
    more » « less