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Neural Pathways of Olfactory Kin Imprinting and Kin Recognition in Zebrafish

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Neural Pathways of Olfactory Kin Imprinting and Kin Recognition in Zebrafish Cell and Tissue Research (2021) 383:273–287 https://doi.org/10.1007/s00441-020-03378-4 REVIEW Neural pathways of olfactory kin imprinting and kin recognition in zebrafish Gabriele Gerlach1,2,3 · Mario F. Wullimann4,5 Received: 8 October 2020 / Accepted: 3 December 2020 / Published online: 30 January 2021 © The Author(s) 2021 Abstract Teleost fsh exhibit extraordinary cognitive skills that are comparable to those of mammals and birds. Kin recognition based on olfactory and visual imprinting requires neuronal circuits that were assumed to be necessarily dependent on the interac- tion of mammalian amygdala, hippocampus, and isocortex, the latter being a structure that teleost fsh are lacking. We show that teleosts—beyond having a hippocampus and pallial amygdala homolog—also have subpallial amygdalar structures. In particular, we identify the medial amygdala and neural olfactory central circuits related to kin imprinting and kin recognition corresponding to an accessory olfactory system despite the absence of a separate vomeronasal organ. Keywords Accessory olfactory system · Amygdala · Crypt cells · Imprinting · Kin recognition · Social behavior · Vomeronasal system Imprinting and kin recognition To reduce potential errors of learning a wrong template is widespread this process of learning mostly occurs early in life when the chances to be with relatives is much higher than later The ability to treat kin diferently from non-kin may be when mobility has increased. Such learning within a narrow achieved by using diferent mechanisms of kin recognition time window and the often life-long memory is called kin and is a key driver for kin selection. One type of kin imprinting. It is used in a wide context of social behavior to recognition is phenotype matching which describes an identify the mother in larger groups, aggregate with siblings, individual learning a template of kin and being able to later cooperate with related conspecifcs for hunting or breeding recognize even unfamiliar kin by matching visual, acoustic, and to avoid inbreeding (Wyatt 2010). or olfactory components of conspecifcs with this template. Organisms can also imprint on a variety of non-conspecifc (Lorenz 1935) and even abiotic objects (Horn 1998). Take the long-known and spectacularly complex home fnding to natal * Mario F. Wullimann streams of adult salmonids. In the fnal stage, this behavior at [email protected] least partially relies on early imprinting on olfactory cues (i.e., Gabriele Gerlach free amino acids) of their place of birth (Ueda 2012; 2019; Bett gabriele.gerlach@uni‑oldenburg.de and Hinch 2016; Ueda et al. 2016; Dittman et al. 1996; Kamran 1 Institute of Biology and Environmental Sciences, Carl-von- et al. 2018; 2019). These early imprinted cues apparently have Ossietzky University, 26129 Oldenburg, Germany nothing to do with kin. Another example are marine Anemone 2 Helmholtz Institute for Functional Marine Biodiversity fshes that live and breed on coral stocks in close proximity of Oldenburg (HIFMB), 26129 Oldenburg, Germany an anemone. The hatchlings are believed to imprint on chemical 3 Centre of Excellence for Coral Reef Studies and School cues of the anemone that they encounter during hatching. After of Marine and Tropical Biology, James Cook University, an open sea planktonic life stage they can use olfactory cues of QLD 4811 Townsville, Australia an anemone to fnd a suitable place for settlement (Arvedlund 4 Graduate School of Systemic Neurosciences & Department and Nielsen 1996). Biology II, Ludwig-Maximilians-Universität Munich, There are various examples of kin-biased behavior and 82152 Planegg‑Martinsried, Germany recognition among teleosts (for review, see Gerlach and 5 Max-Planck-Institute for Neurobiology, Hinz 2012), mostly revealed by behavioral experiments. 82152 Planegg‑Martinsried, Germany Vol.:(0123456789)1 3 274 Cell and Tissue Research (2021) 383:273–287 A few examples shall illustrate this point: mangrove Zebrafish kin related behavior and olfactory killifsh prefer to associate with their kin (Edenbrow and periphery Croft 2012). Larval guppies (poecilids) can distinguish kin from non-kin (Hain and Nef 2007; Hain et al. 2017) and Zebrafish kin imprinting and kin recognition tend to form shoals with siblings (Piyapong et al. 2011). Closely related mollies (also poecilids) associate with kin Research in zebrafsh represents one of the best-defned and using visual and chemical cues (both alone are sufcient) most coherently documented cases of imprinting on kin and show aggressive behavior towards non-kin (Makowicz and kin recognition in vertebrates. This work ranges from et al. 2016). These three cases represent cyprinodontiforms. behavioral experiments, molecular genetics, immunohisto- Also, salmoniform brook trouts form kin groups early, chemical identifcation of underlying neural structures at but dissolve when approaching the breeding stage (Meli peripheral and central nervous levels, neuronal tract-tracing and Fraser 2013). Brown trout fry (O’Farrell et al. 2012) of pathways involved, as well as experimental activation of and Atlantic salmon juveniles (Rajakaruna et al. 2006) neuronal structures along these pathways using the neuronal associate with kin as shown by MHC class I or MHC class activity related marker phosphorylated extracellular signal II allele similarity, respectively. Within perch-like fshes, regulated kinase (pERK). male adult bluegill sunfishes (Lepomis macrochirus) The behavioral aspects of kin imprinting, the general recognize “their” newly hatched ofspring using chemical olfactory epithelial sensory cell composition, their receptor cues (Nef 2003) and their ofspring later recognizes kin molecules and—if known—ligands, their diferential pri- from non-kin (Hain and Nef 2006). Adult male cichlids mary projections to the olfactory bulb, as well as the analysis (Pelvicachromis taeniatus) prefer their own odor over that of which sensory cells and olfactory glomeruli are involved of other individuals (Thünken et al. 2009) and larva show in kin imprinting and recognition have been reviewed greater group cohesion with kin than with other individuals, recently by Gerlach and colleagues (Gerlach et al. 2019). but cohesion decreases with elevated competition (Hesse Thus, these topics will be only briefy introduced here. and Thünken 2014; Thünken et al. 2020). In another cichlid Depending on temperature (25°C), zebrafish larvae (Neolamprologus caudopunctatus), small females tend to hatch from the chorion at day 4 dph and 5 dph (days form shoals with kin while larger individuals disperse (van posthatching). Shortly thereafter, the imprinting process Dongen et al. 2014; review on cichlids by Keller-Costa starts while larvae are only starting to be mobile. Larvae et al. 2015). Adult female sticklebacks diferentiate male kin that were exposed to the visual cues of siblings at 5 dph from non-kin based on olfaction alone (Mehlis et al. 2008), and at 6 dph to olfactory cues of siblings that shared the whereas in male aggressive interplays, no diference in same MHC class II alleles became imprinted on siblings. behavior is apparent towards kin or non-kin males (Mehlis An olfactory preference for siblings is the result when et al. 2009). In some cypriniforms (such as the zebrafsh, see zebrafish were still sexually immature juveniles, but as below), larval shoaling based on kin recognition is present. adults, females avoided the scent of brothers and males Kin recognition-based group association has been suggested were interested in olfactory and visual cues of females, recently in two coral reef living species of damselfish but did not care about relatedness (Gerlach and Lysiak (percomorph pomacentrids) (Miller-Sims et al. 2008; Buston 2006). These time windows for imprinting on visual et al. 2009; review Gerlach et al. 2019). Regarding the and olfactory cues are short and last only for 1 to 2 days special case of kin recognition in the context of shoaling, an (Gerlach et al. 2008). If imprinting does not occur during important issue is to test whether experimental results mimic this period, zebrafish do not express any kin recognition naturally occurring kin groupings (Krause et al. 2000). later on. Interestingly, larvae only imprint on kin but In any case, these examples from taxa as diverse not on non-kin cues; when they were exposed to visual as salmoniforms, cypriniforms, gasterosteiforms, or olfactory cues of non-kin during this sensitive phase, cyprinodontiforms or cichliforms and other percomorphs they did not imprint and do not show any preference for are clear evidence that kin recognition is widespread among the experienced non-kin (Hinz et al. 2013a). The only freshwater and maybe marine teleosts. However, although it exception occurs when non-kin share the same MHC is likely that this “knowledge” about kin relationship arises class II alleles with the zebrafish larvae. In this case, during early life history through a process of imprinting, zebrafish imprinted on MHC class II identical zebrafish details on the involved peripheral sensory mechanism, let non-kin larvae and showed a preference for kin later alone on the central neural underpinnings of imprinting and in life (Hinz et al. 2013b). To understand the chemical kin recognition are notoriously evasive in all these cases. In composition of the olfactory cues, we tested larvae from contrast, the beauty of the zebrafsh example is that we have a different zebrafish pairs and MHC class II alleles for good understanding of the entire life-history of
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