Crypt cells are involved in kin recognition in larval zebrafish

Abstract

Zebrafish larvae imprint on visual and olfactory kin cues at day 5 and 6 postfertilization, respectively, resulting in kin recognition later in life. Exposure to non-kin cues prevents imprinting and kin recognition. Imprinting depends on MHC class II related signals and only larvae sharing MHC class II alleles can imprint on each other. Here, we analyzed which type of olfactory sensory neuron (OSN) detects kin odor. The single teleost olfactory epithelium harbors ciliated OSNs carrying OR and TAAR gene family receptors (mammals: main olfactory epithelium) and microvillous OSNs with V1R and V2R gene family receptors (mammals: vomeronasal organ). Additionally, teleosts exhibit crypt cells which possess microvilli and cilia. We used the activity marker pERK (phosphorylated extracellular signal regulated kinase) after stimulating 9 day old zebrafish larvae with either non-kin conspecific or food odor. While food odor activated both ciliated and microvillous OSNs, only the latter were activated by conspecific odor, crypt cells showed no activation to both stimuli. Then, we tested imprinted and non-imprinted larvae (full siblings) for kin odor detection. We provide the first direct evidence that crypt cells, and likely a subpopulation of microvillous OSNs, but not ciliated OSNs, play a role in detecting a kin odor related signal.

Identification of accessory olfactory system and medial amygdala in the zebrafish

“…These activity differences in the zebrafish medial amygdala (intermediate nucleus of ventral telencephalon) in comparisons of imprinted and non-imprinted zebrafish larvae are highly exciting and clearly call for further investigation in particular with respect to additional inputs from microvillous cells. As reported before, in addition to the ubiquitous activation of crypt cells, a small subpopulation of microvillous olfactory sensory neurons was also activated by kin odor39.…”

“…However, it had been established recently in the zebrafish that one receptor is present in all crypt cells (the V1R type receptor ora4 which is associated with Gαi;11) and that they project into the single S100-positive glomerulus located in the mediodorsal olfactory bulb, the mdG291014 (see Introduction). In addition, we have provided new data on neuronal activation using pERK suggesting a role of crypt cells in kin recognition39. These studies involved experimentally raised imprinted and non-imprinted zebrafish larvae (see Fig.…”

“…5), followed by histological processing for detection of neuronal activation has been described in detail already39. Briefly, we recapitulate these issues below.…”

Odorant organization in the olfactory bulb of the sea lamprey

“…In the current study, label application was confined to the medial glomerular region containing the dendrites and cell bodies on the medial projection neurons that extend to the posterior tuberculum (Green et al, 2013) and the retrogradely labelled sensory neurons were restricted to the accessory olfactory organ. The short, rounded shape of these sensory neurons matched the morphology reported by Ren et al (2009), and is similar to crypt cells that project to the lateral margin of the olfactory bulb in lungfish (Gonzalez et al, 2010) and to crypt cells distributed throughout the olfactory epithelium and projecting to dorso-medial glomeruli in the zebrafish olfactory bulb (Gayoso et al, 2012;Ahuja et al, 2013;Biechl et al, 2016).…”

Mechanosensory signaling as a potential mode of communication during social interactions in fishes

“…Although chemosensory communication is thought to be the primary sense involved in kin recognition in fishes (salmonids: Olsén, 1992; zebrafish: Biechl et al, 2016), evidence suggests that parents also employ mechanosensory communication to signal to their offspring. In some species, parents 'call' to their young using abrupt raising and lowering of various fins and occasional tailbeating (Baerends and Baerends-van Roon, 1950;Fryer and Iles, 1972).…”