4Terrestrial animals compute shortcuts through their environment by integrating self-5 motion vectors containing distance and direction information. The sensory and neural 6 mechanisms underlying this navigational feat have been extensively documented, but their 7 evolutionary origins remain unexplored. Among extant vertebrates, the teleost fish make up 8 one of the most diverse and earliest-branching phylogenetic groups, and provide a powerful 9 system to study the origins of vertebrate spatial processing. However, how freely-swimming 10 teleost fish collect and compute metric spatial information underwater are unknown. Using 11 the Picasso triggerfish, Rhinecanthus aculeatus, we investigate the functional and mechanis-12 tic basis of distance estimation in teleost fish for the first time. We show that a fish can 13 learn and remember distance travelled with remarkable accuracy. By analysing swimming 14 trajectories, we form hypotheses about how distance is represented in the teleost brain, and 15 propose that distance may be encoded by dedicated neural structures in a similar way to ter-16 restrial vertebrates. Finally, we begin exploring the sensory mechanisms underlying distance 17 estimation in fish. Many walking animals use a step counter for odometry. By quantifying 18 finbeat use during our distance task, we show that a functionally equivalent finbeat counter 19 is unlikely to provide reliable and precise distance information in an aquatic environment. 20 1 1 Background 21 A powerful way for an animal to navigate through its environment is through path integration.
22Self-movement vectors containing distance and direction information are constantly and auto-23 matically summated throughout any journey, providing the animal with an internal store of a 24 vector taking it directly back to a starting position [1, 2]. The result is a dramatic increase in 25 navigation efficiency -shortcuts can be constructed through entirely unexplored terrain, avoiding 26 the need to use external information to retrace previous steps.
27To achieve this navigational feat, an animal must have dedicated sensory mechanisms and 28 neural structures to collect and process distance and direction information from self-motion cues.
29Such mechanisms have been extensively studied in terrestrial animals ranging from mammals such 30 as humans [3] and rats [4, 5], and invertebrates such as spiders [6], ants [7], and bees [8, 9].
31In contrast, how underwater species collect, process, and use metric spatial information to ac-32 curately navigate through their environment is largely unknown. An aquatic habitat is a fascinat-33 ing environment to navigate through from a sensory and computational point of view. It contains 34 sensory information not available on land, such as hydrodynamic cues from water flow, hydro-35 static pressure from above, and electric currents carried through the water. Freely-swimming 36 animals also have six degrees of freedom of movement (3 translational: forwards/backwards, 37 left/right, up/down; 3 rotationa...