High-throughput simulations indicate feasibility of navigation by familiarity with a local sensor such as scorpion pectines

Abstract

Scorpions have arguably the most elaborate "tongues" on the planet: two paired ventral combs, called pectines, that are covered in thousands of chemo-tactile peg sensilla and that sweep the ground as the animal walks. Males use their pectines to detect female pheromones during the mating season, but females have pectines too: What additional purpose must the pectines serve? Why are there so many pegs? We take a computational approach to test the hypothesis that scorpions use their pectines to navigate by chemo-textural familiarity in a manner analogous to the visual navigation-by-scene-familiarity hypothesis for hymenopteran insects. We have developed a general model of navigation by familiarity with a local sensor and have chosen a range of plausible parameters for it based on the existing behavioral, physiological, morphological, and neurological understanding of the pectines. Similarly, we constructed virtual environments based on the scorpion's native sand habitat. Using a novel methodology of highly parallel high-throughput simulations, we comprehensively tested 2160 combinations of sensory and environmental properties in each of 24 different situations, giving a total of 51,840 trials. Our results show that navigation by familiarity with a local pectine-like sensor is feasible. Further, they suggest a subtle interplay between "complexity" and "continuity" in navigation by familiarity and give June 10, 2020 1/34 the surprising result that more complexity -more detail and more information -is not always better for navigational performance. Author summaryScorpions' pectines are intricate taste-and-touch sensory appendages that brush the ground as the animal walks. Pectines are involved in detecting pheromones, but their exquisite complexity -a pair of pectines can have around 100,000 sensory neuronssuggests that they do more. One hypothesis is "Navigation by Scene Familiarity," which explains how bees and ants use their compound eyes to navigate home: the insect visually scans side to side as it moves, compares what it sees to scenes learned along a training path, and moves in the direction that looks most familiar. We propose that the scorpions' pectines can be used to navigate similarly: instead of looking around, they sweep side to side sensing local chemical and textural information. We crafted simulated scorpions based on current understanding of the pectines and tested their navigational performance in virtual versions of the animals' sandy habitat. Using a supercomputer, we varied nine environmental, sensory, and situational properties and ran a total of 51,840 trials of simulated navigation. We showed that navigation by familiarity with a local sensor like the pectines is feasible. Surprisingly, we also found that having a more detailed landscape and/or a more sensitive sensor is not always optimal.Introduction 1 Scorpions present at least two unanswered scientific mysteries: the selection pressure 2 that maintains their pectines -two ornate, sensitive, and energetically expensive 3 sensory organs on t...

Synaptic Interactions in Scorpion Peg Sensilla Appear to Maintain Chemosensory Neurons within Dynamic Firing Range

“…The Navigation by Chemotextural Familiarity Hypothesis [9,10,42] predicts that scorpions use path integration or learning walks to acquire home-directed chemo-tactile information using the matrices of peg sensilla on their pectines. Then, during subsequent journeys they recapitulate these paths by comparing current pectinal "tastes" and "textures" with those most "familiar" in memory and moving in that direction.…”

“…Nightly hunting excursions take scorpions far away from their burrows, but they still find a way to return to them. The Navigation by Chemotextural Familiarity Hypothesis (NCFH) suggests that scorpions learn chemical and textural information gathered when the pectines brush against the ground that is used during subsequent returns home [9,10].…”

“…However, both male and female scorpions have pectines, and this synaptic interaction is present in peg sensilla of both sexes [2]. The NCFH suggests that the matrices of peg sensilla on pectines are important for acquiring accurate chemical and textural information about their habitat [9,10]. There is also evidence that scorpions use their pectines to track prey [6,22].…”

Structure of the pecten neuropil pathway and its innervation by bimodal peg afferents in two scorpion species

“…It has further been proposed that scorpions use path integration without the necessity of visual input during homing [ 91 ]. The pectines seem to be involved in navigation in general and homing in particular, by using scene familiarity detected by the peg sensillae [ 92 , 93 ].…”

Evidence of learning walks related to scorpion home burrow navigation

“…We have developed proof-of-concept models of how scorpions could navigate using ground-based information acquired by their pectines (similar to models of visual navigation in ants; Baddeley et al, 2012 ). We have termed this process ‘navigation by chemo-textural familiarity’ ( Gaffin and Brayfield, 2017 ; Musaelian and Gaffin, 2020 preprint). Put simply, to get home, the scorpion uses its pectines to detect and move toward tastes and textures it has learned during previous home-bound forays.…”