Ontogeny and Sexual Differences in Swimming Proximity to Conspecifics in Response to Visual Cues in Medaka Fish

Abstract

Adult medaka fish (Oryzias latipes) exhibit complex social behaviors that depend mainly on visual cues from conspecifics. The ontogeny of visually-mediated social behaviors from larval/juvenile to adult medaka fish, however, is unknown. In the present study, we established a simple behavioral paradigm to evaluate the swimming proximity to conspecifics based on visual cues in an inter-individual interaction of two medaka fish throughout life. When two fish were placed separately in a cylindrical tank with a concentric transparent wall, the two fish maintained close proximity to each other. A normal fish inside the tank maintained proximity to an optic nerve-cut fish outside of the tank, while the converse was not true. This behavioral paradigm enabled us to quantify visually-induced motivation of a single fish inside the tank. The proximity was detected from larval/juvenile to adult fish. Larval fish, however, maintained close proximity not only to conspecifics, but also to heterospecifics. As the growth stage increased, the degree of proximity to heterospecifics decreased, suggesting that shoaling preferences toward conspecifics and/or visual ability to recognize conspecifics is refined and established according to the growth stage. Furthermore, the proximity of adult female fish was affected by their reproductive status and social familiarity. Only before spawning, adult females maintained closer proximity to familiar males rather than to unfamiliar males, suggesting that proximity was affected by familiarity in a female-specific manner. This simple behavioral paradigm will contribute to our understanding of the neural basis of the development of visually-mediated social behavior using medaka fish.

Molecular basis of social competence in medaka fish

“…Medaka females have the ability to discriminate a visually familiar male from an unfamiliar male (Isoe et al . ). Unlike guppies, medaka females prefer to mate with familiar males (Okuyama et al .…”

“…Visual familiarization, that is, the process of becoming familiar with an individual through visual contact, affects female mate preference in medaka fish. Medaka females have the ability to discriminate a visually familiar male from an unfamiliar male (Isoe et al 2016). Unlike guppies, medaka females prefer to mate with familiar males Yokoi et al 2016).…”

“…Recently, medaka fish, Oryzias latipes, a popular pet for hundreds of years in Japan, have been used to study the molecular/neural basis of fish social behavior (Fukamachi et al 2009;Imada et al 2010;Kagawa 2013;Ochiai et al 2013;Nakayasu & Watanabe 2014;Okuyama et al 2014;Tsuboko et al 2014;Yokoi et al 2015Yokoi et al , 2016Isoe et al 2016;Utagawa et al 2016). The medaka genome-sequencing project is complete (Kasahara et al 2007;Kobayashi & Takeda 2008) and state-of-the-art technologies for molecular genetics studies, such as genome editing (Ansai et al 2013;Ansai & Kinoshita 2014) and conditional gene manipulation (Okuyama et al 2013;Ansai et al 2016), are available, allowing for detailed dissection of molecular/neural functions.…”

Three-dimensional computer graphic animations for studying social approach behaviour in medaka fish: Effects of systematic manipulation of morphological and motion cues

“…Many researchers have analysed shoaling and schooling-like behaviours in medaka fish [14–21], and medaka were dependent on visual cues to maintain proximity to conspecifics [15, 21] or mirror images of their own selves [17]. However, the detailed nature of visual attraction in medaka remains unclear.…”

TMT-Opsins differentially modulate medaka brain function in a context-dependent manner

“…As the expression domains of tmt-opsin1b nor tmt-opsin2 do not observably change between young larvae and adults [14], we think that the most plausible explanation for the agedependency is the still on-going differentiation of the nervous system during young larval stages. Ontogenetic changes in behavior are very common and for instance well documented for the visual processing and social behavior in medaka fish [53,59]. While the cellular and molecular causes still remain to be determined, it is clear that the phenomenon is common among vertebrates and even extends to humans across lifespan, where it has been shown to correlate with changes in glutamatergic and GABAergic systems [60,61].…”