Ontogeny of Inner Ear Saccular Development in the Plainfin Midshipman (Porichthys notatus)

Abstract

The auditory system of the plainfin midshipman fish (<i>Porichthys notatus</i>) is an important sensory system used to detect and encode biologically relevant acoustic stimuli important for survival and reproduction including social acoustic signals used for intraspecific communication. Previous work showed that hair cell (HC) density in the midshipman saccule increased seasonally with reproductive state and was concurrent with enhanced auditory saccular sensitivity in both females and type I males. Although reproductive state-dependent changes in HC density have been well characterized in the adult midshipman saccule, less is known about how the saccule changes during ontogeny. Here, we examined the ontogenetic development of the saccule in four relative sizes of midshipman (larvae, small juveniles, large juveniles, and nonreproductive adults) to determine whether the density, total number, and orientation patterns of saccular HCs change during ontogeny. In addition, we also examined whether the total number of HCs in the saccule differ from that of the utricle and lagena in nonreproductive adults. We found that HC density varied across developmental stage. The ontogenetic reduction in HC density was concurrent with an ontogenetic increase in macula area. The orientation pattern of saccular HCs was similar to the standard pattern previously described in other teleost fishes, and this pattern of HC orientation was retained during ontogeny. Lastly, the estimated number of saccular HCs increased with developmental stage from the smallest larvae (2,336 HCs) to the largest nonreproductive adult (145,717 HCs), and in nonreproductive adults estimated HC numbers were highest in the saccule (mean ± SD = 28,479 ± 4,809 HCs), intermediate in the utricle (mean ± SD = 11,008 ± 1,619 HCs) and lowest in the lagena (mean ± SD = 4,560 ± 769 HCs).

Ontogenetic development of inner ear hair cell organization in the New Zealand carpet shark Cephaloscyllium isabellum

“…Linear ontogenetic increases in macular area and HCT were also documented in the saccule, lagena, and utricle of G. galeus, the only other ontogenetic study of inner ear HCs in elasmobranch otolith organs (Sauer et al, 2022). Studies on various otolith organs of bony fishes have also reported ontogenetic increases in macular area and HCT (Popper and Hoxter, 1984;Lombarte and Popper, 1994;Higgs et al, 2002Higgs et al, , 2003Chaves et al, 2017;Lozier and Sisneros, 2020). While the functional significance of these ontogenetic changes is unclear, it has been suggested that increasing HCT may enhance auditory sensitivity as fishes grow (Corwin, 1983;Coffin et al, 2012;Lu and Desmidt, 2013;Wang et al, 2015) or could act to maintain stable hearing throughout ontogeny (Popper et al, 1988;Rogers et al, 1988;Higgs et al, 2003).…”

“…The smaller size range of C. isabellum (∼20-90 cm) compared to G. galeus (∼30-170 cm) might minimize ontogenetic changes in HCD, although Corwin (1977Corwin ( , 1981a reported no differences in HCD of the macula neglecta between juvenile and adult blacktip and gray reef sharks (Carcharhinus melanopterus and Carcharhinus amblyrhynchos, respectively), two species with similar size ranges to G. galeus. There is likely variation in HCD patterns between elasmobranchs, similar to in bony fishes, where data indicate that ontogenetic changes in HCD may be species-specific, macula-specific, and even dependent on developmental stage (Popper and Hoxter, 1984;Lombarte and Popper, 1994;Higgs et al, 2002;Lu and Desmidt, 2013;Wang et al, 2015;Chaves et al, 2017;Lozier and Sisneros, 2020). Further quantification of HCD across full size ranges and in all inner ear maculae, especially in elasmobranchs, is needed to characterize postembryonic development of HCD in fishes.…”

“…In C. isabellum, the significant differences in macular area, HCT, and HCD between the four maculae indicate that some maculae have distinct characteristics that may relate to specific roles in auditory and/or vestibular function. While the relative importance of these different characteristics (macular area, HCT, HCD) to inner ear function is unknown, differences in HC number and/or density may relate to auditory capacity (Corwin, 1983;Coffin et al, 2012;Lu and Desmidt, 2013;Wang et al, 2015;Chaves et al, 2017;Lozier and Sisneros, 2020). Accordingly, the utricle and saccule, which exhibited a relatively large size, HC number, and HC density in C. isabellum, may possess greater sensitivity to acoustical displacements compared to the other maculae.…”

“…Moreover, the inner ears (including HCs) of fishes grow indeterminately (Corwin, 1983;Popper and Hoxter, 1984;Lombarte and Popper, 1994) and thus provide a unique opportunity to understand ontogenetic changes in the inner ear that may underlie changes in auditory capabilities throughout life in aquatic vertebrates. Despite this, only a handful of studies have investigated ontogenetic development of HCs in fishes (e.g., Corwin, 1983;Popper and Hoxter, 1984;Lombarte and Popper, 1994;Higgs et al, 2002;Wang et al, 2015;Chaves et al, 2017;Lozier and Sisneros, 2020;Sauer et al, 2022).…”

“…In fishes, growth of the inner ear is generally characterized by an increase in macula size and an increase in absolute number of HCs (Corwin, 1983;Popper and Hoxter, 1984;Lombarte and Popper, 1994;Chaves et al, 2017;Lozier and Sisneros, 2020;Sauer et al, 2022), decreasing density of HCs (Coffin et al, 2012;Chaves et al, 2017;Lozier and Sisneros, 2020;Sauer et al, 2022), and HC orientation groups that do not change (Lombarte and Popper, 1994;Chaves et al, 2017;Lozier and Sisneros, 2020;Sauer et al, 2022). While evidence for the functional significance of these changes is limited and inconsistent (Corwin, 1983;Higgs et al, 2002Higgs et al, , 2003Coffin et al, 2012;Lu and Desmidt, 2013;Wang et al, 2015), it seems likely that changes to the sensory epithelia will impact some aspect of auditory and/or vestibular capacity.…”