Whole-head recording of chemosensory activity in the marine annelid Platynereis dumerilii.

Thomas F Chartier,Detlev Arendt,Gáspár Jékely,Wiebke Dürichen,Joran Deschamps

doi:10.1098/rsob.180139

Thomas F Chartier, Detlev Arendt + Show 3 more

Open Access

https://doi.org/10.1098/rsob.180139

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Abstract

Chemical detection is key to various behaviours in both marine and terrestrial animals. Marine species, though highly diverse, have been underrepresented so far in studies on chemosensory systems, and our knowledge mostly concerns the detection of airborne cues. A broader comparative approach is therefore desirable. Marine annelid worms with their rich behavioural repertoire represent attractive models for chemosensation. Here, we study the marine worm Platynereis dumerilii to provide the first comprehensive investigation of head chemosensory organ physiology in an annelid. By combining microfluidics and calcium imaging, we record neuronal activity in the entire head of early juveniles upon chemical stimulation. We find that Platynereis uses four types of organs to detect stimuli such as alcohols, esters, amino acids and sugars. Antennae are the main chemosensory organs, compared to the more differentially responding nuchal organs or palps. We report chemically evoked activity in possible downstream brain regions including the mushroom bodies (MBs), which are anatomically and molecularly similar to insect MBs. We conclude that chemosensation is a major sensory modality for marine annelids and propose early Platynereis juveniles as a model to study annelid chemosensory systems.

Highlights

Chemical signals are central to animal behaviour, including feeding, predation, courtship and mating, aggregation, defence, habitat selection and communication [1]
We report here a comprehensive study of head chemosensory organ physiology in the marine annelid Platynereis dumerilii, which can be kept in the laboratory and is amenable to molecular studies
We found that nuchal organs, palps, antennae and tentacular cirri are chemosensory, though with different degrees of specialization: for example, antennae responded to all stimulants, while nuchal organs were most sensitive to amyl acetate and sucrose, but did not respond to glutamate

Summary

Introduction

Chemical signals are central to animal behaviour, including feeding, predation, courtship and mating, aggregation, defence, habitat selection and communication [1]. Adapting to variable habitats and changing chemical landscapes, animals have evolved a broad variety of chemosensory organs. Genomic studies have revealed that receptor proteins are highly diverse in the animal kingdom [7] and can be entirely different between distant species—vertebrates and insects, for example, use distinct types of receptors [8,9]. A broader comparative approach will facilitate the elucidation of both general operating principles and evolutionary origins of animal chemosensation. Notwithstanding studies in fish and crustaceans [10,11], and to a lesser extent in molluscs [12,13], our current understanding of animal chemosensation still mainly concerns terrestrial and airborne cues.

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