Reproductive and metabolic state differences in olfactory responses to amino acids in a mouth brooding African cichlid fish

Abstract

Olfaction mediates many crucial life-history behaviors such as prey detection, predator avoidance, migration and reproduction. Olfactory function can also be modulated by an animal's internal physiological and metabolic states. While this is relatively well studied in mammals, little is known about how internal state impacts olfaction in fishes, the largest and most diverse group of vertebrates. Here we apply electro-olfactograms (EOGs) in the African cichlid fish to test the hypothesis that olfactory responses to food-related cues (i.e. l-amino acids; alanine and arginine) vary with metabolic, social and reproductive state. Dominant males (reproductively active, reduced feeding) had greater EOG magnitudes in response to amino acids at the same tested concentration than subordinate males (reproductively suppressed, greater feeding and growth rates). Mouth brooding females, which are in a period of starvation while they brood fry in their mouths, had greater EOG magnitudes in response to amino acids at the same tested concentration than both recovering and gravid females that are feeding. Discriminant function analysis on EOG magnitudes also grouped the male (subordinate) and female (recovering, gravid) phenotypes with higher food intake together and distinguished them from brooding females and dominant males. The slope of the initial negative phase of the EOG also showed intra-sexual differences in both sexes. Our results demonstrate that the relationship between olfaction and metabolic state observed in other taxa is conserved to fishes. For the first time, we provide evidence for intra-sexual plasticity in the olfactory response to amino acids that is influenced by fish reproductive, social and metabolic state.

A central control circuit for encoding perceived food value

“…Similar fine tuning of sensory processing in the leech has been implicated in the altered perception of stimuli in other statedependent decisions (Gaudry and Kristan, 2009). Likewise, in comparable vertebrate paradigms, hunger state modulates sensory neuron firing properties in response to a stimulus (Breunig et al, 2010;Negroni et al, 2012;Nikonov et al, 2017). In all cases, for these relatively simple decisions where the animal is changing its responsiveness as a means to drive graded increases or decreases in behavior, sensory retuning is apparently an effective solution.…”

Internal amino acid state modulates yeast taste neurons to support protein homeostasis inDrosophila

“…Intriguingly, acute blockade of synaptic release from these neuromodulatory systems did not suppress yeast appetite induced by yeast deprivation (Supplementary Table 1), suggesting that a distinct mechanism may regulate sensory gain according to AA state. Alternatively, this modulation could occur at the level of peripheral sensory responses, as seen for AA responses in the fish olfactory and locust gustatory systems 79,80 . In Significance was tested using two-way ANOVA, with deprivation and mating states as the independent variables.…”

Social Recognition and Social Attraction in Group-Living Fishes

“…The mix of chemicals contributing to a fish's chemical signature represent a continually changing representation of both intrinsic factors, such as their physiological state, and extrinsic factors, such as the animal's environment or diet (Henneken et al, 2017;Nikonov et al, 2017). These cues are known to affect association preferences with fish preferring to shoal with individuals that smell most like themselves, which clearly implicates self-referent phenotype matching as the mechanism.…”