Gene expression underlying enhanced, steroid-dependent auditory sensitivity of hair cell epithelium in a vocal fish

Abstract

BackgroundSuccessful animal communication depends on a receiver’s ability to detect a sender’s signal. Exemplars of adaptive sender-receiver coupling include acoustic communication, often important in the context of seasonal reproduction. During the reproductive summer season, both male and female midshipman fish (Porichthys notatus) exhibit similar increases in the steroid-dependent frequency sensitivity of the saccule, the main auditory division of the inner ear. This form of auditory plasticity enhances detection of the higher frequency components of the multi-harmonic, long-duration advertisement calls produced repetitively by males during summer nights of peak vocal and spawning activity. The molecular basis of this seasonal auditory plasticity has not been fully resolved. Here, we utilize an unbiased transcriptomic RNA sequencing approach to identify differentially expressed transcripts within the saccule’s hair cell epithelium of reproductive summer and non-reproductive winter fish.ResultsWe assembled 74,027 unique transcripts from our saccular epithelial sequence reads. Of these, 6.4 % and 3.0 % were upregulated in the reproductive and non-reproductive saccular epithelium, respectively. Gene ontology (GO) term enrichment analyses of the differentially expressed transcripts showed that the reproductive saccular epithelium was transcriptionally, translationally, and metabolically more active than the non-reproductive epithelium. Furthermore, the expression of a specific suite of candidate genes, including ion channels and components of steroid-signaling pathways, was upregulated in the reproductive compared to the non-reproductive saccular epithelium. We found reported auditory functions for 14 candidate genes upregulated in the reproductive midshipman saccular epithelium, 8 of which are enriched in mouse hair cells, validating their hair cell-specific functions across vertebrates.ConclusionsWe identified a suite of differentially expressed genes belonging to neurotransmission and steroid-signaling pathways, consistent with previous work showing the importance of these characters in regulating hair cell auditory sensitivity in midshipman fish and, more broadly, vertebrates. The results were also consistent with auditory hair cells being generally more physiologically active when animals are in a reproductive state, a time of enhanced sensory-motor coupling between the auditory periphery and the upper harmonics of vocalizations. Together with several new candidate genes, our results identify discrete patterns of gene expression linked to frequency- and steroid-dependent plasticity of hair cell auditory sensitivity.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1940-3) contains supplementary material, which is available to authorized users.

Saccular Transcriptome Profiles of the Seasonal Breeding Plainfin Midshipman Fish (Porichthys notatus), a Teleost with Divergent Sexual Phenotypes

“…These differences may reflect seasonal auditory changes, or may be a result of the different habitats where these fish were collected, as all reproductive fishes were obtained from shallow-water nests while winter females were collected via trawls in deeper water. Our data are consistent with a recent study that found significant up-regulation of metabolic transcripts, including protein synthesis genes, in the inner ears of type I male reproductive midshipman fish [ 69 ]. However, that study did not examine type II males, which occupy a unique transcriptional niche in our dataset.…”

Age‐related hearing loss: Why we need to think about sex as a biological variable

“…Therefore, it is tempting to hypothesize that the molecular pathways that are important for sex-specific modulation of the auditory system during mating behavior in nonhumans, and are conserved across species, are the ones that will manifest in humans in sexspecific susceptibility to complex disease like ARHL. In fish, there is already some evidence to support this concept (Fergus et al, 2015).…”

“…In other species, including birds (Krentzel & Remage-Healey, 2015), fish (Fergus, Feng, Feng, & Bass, 2015), anuran amphibians (frogs/toads) (Shen et al, 2011), and mosquitoes (Su et al, 2018), sex-specific differences in auditory sensitivity are coupled to reproduction and linked to the acoustic communication essential for courtship behavior (see also the excellent review by (Caras, 2013). Even in humans we can draw parallels between reproduction and auditory function because auditory sensitivity in women fluctuates during the menstrual cycle, with an enhanced auditory sensitivity coinciding with the time of ovulation.…”

“…Genes that are correlated with auditory tuning during mating in a teleost fish, the midshipman fish, are enriched in metabolic pathways involving ion channels, neurotransmission, and steroid signaling. Two of these genes are members of the ERR family, ESRRB and ESRRG (Fergus et al, 2015). The former (ESRRB) is a gene already linked with susceptibility to noise exposure in humans (Bhatt et al, 2016), and the latter (ESRRG) is a gene already linked with susceptibility to ARHL in women (Nolan, Maier, et al, 2013).…”

Forebrain Dopamine System Regulates Inner Ear Auditory Sensitivity to Socially Relevant Acoustic Signals

“…Whereas mammals possess five dopamine receptor subtypes, teleost fishes may possess genes for up to fourteen receptor subtypes as a consequence of genome duplication events [32]. Utilizing transcriptomes of the midshipman saccule [33,34], we identified transcripts for seven dopamine receptor subtypes (Figure S3). Due to the seasonal differences of dopamine fiber innervation [19] and the effects of dopamine on saccular sensitivity (Figures 2 and 3), we hypothesized that dopamine receptor expression would be seasonally labile.…”