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ABSTRACT Plainfin midshipman fish (Porichthys notatus) exhibit seasonal auditory plasticity that enhances their reproductive success. During the summer, type I male midshipman acoustically court females and both the males and females exhibit increased auditory sensitivity during this period. The enhanced auditory sensitivity is associated with increased density of sensory hair cells in the saccule but not the utricle, suggesting that different mechanisms underlie physiological plasticity in distinct inner ear regions. To better understand how shifts in hair cell number occur within auditory tissues, we examined cell turnover across breeding states and sexes in midshipman fish. We found that reproductive type I males exhibited less saccular cell proliferation than non-reproductive males without a change in cell death, indicating a net loss of saccular cells during the breeding season. By contrast, saccular cell proliferation increased in summer females, with no seasonal changes in other inner ear epithelia. Collectively, our data reveal that multiple mechanisms are likely to contribute to seasonal auditory plasticity within a single species, potentially within the ear of an individual animal. 

ABSTRACT Successful plant growth requires plants to minimize harm from antagonists and maximize benefit from mutualists. However, these outcomes may be difficult to achieve simultaneously, since plant defenses activated in response to antagonists can compromise mutualism function, and plant resources allocated to defense may trade off with resources allocated to managing mutualists. Here, we investigate how antagonist attack affects plant ability to manage mutualists with sanctions, in which a plant rewards cooperative mutualists and/or punishes uncooperative mutualists. We studied interactions among wild and domesticated pea plants, pea aphids, an aphid‐vectored virus (Pea Enation Mosaic Virus, PEMV), and mutualistic rhizobial bacteria that fix nitrogen in root nodules. Using isogenic rhizobial strains that differ in their ability to fix nitrogen and express contrasting fluorescent proteins, we found that peas demonstrated sanctions in both singly‐infected nodules and mixed‐infection nodules containing both strains. However, the plant's ability to manage mutualists in mixed‐infection nodules traded off with its ability to defend against antagonists: when plants were attacked by aphids, they stopped sanctioning within mixed‐infection nodules, and plants that exerted stricter sanctions within nodules during aphid attack accumulated higher levels of the aphid‐vectored virus, PEMV. Our findings suggest that plants engaged in defense against antagonists suffer a reduced ability to select for the most beneficial symbionts in mixed‐infection tissues. Mixed‐infection tissues may be relatively common in this mutualism, and reduced plant sanctions in these tissues could provide a refuge for uncooperative mutualists and compromise the benefit that plants obtain from mutualistic symbionts during antagonist attack. Understanding the conflicting selective pressures plants face in complex biotic environments will be crucial for breeding crop varieties that can maximize benefits from mutualists even when they encounter antagonists. 

Most of us have heard birds sing during the spring breeding season. Did you know that some fish also sing to attract mates? We study plainfin midshipman fish, a fascinating fish that makes its home along the Pacific Coast of North America. The big male fish sing during the summer months and their sound-producing muscles get bigger in the summer, probably to make them sound more attractive to females. Female midshipman fish go through seasonal changes, too. In the summer their hearing improves, which helps them pick the right male to mate with. We study hearing in female plainfin midshipman, measuring how their ears respond to sound and how the number of hearing cells in their ears changes between winter and summer. We want to know how seasonal changes in hormones affect hearing in this “songbird of the sea”. 

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.