Thermotaxis in an apolar, non-neuronal animal

Abstract

Neuronal circuits are hallmarks of complex decision making processes in the animal world. How animals without neurons process information and respond to environmental cues promises a new window into studying precursors of neuronal control and origin of the nervous system as we know it today. Robust decision making in animals, such as in chemotaxis or thermotaxis, often requires internal symmetry breaking (such as A-P axis) provided naturally by a given body plan of an animal. Here we report the discovery of robust thermotaxis behavior in Trichoplax adhaerens, an early divergent, enigmatic animal with no anterior-posterior symmetry breaking (apolar), and no known neurons or muscles. We present the first quantitative and robust behavioral response assay in placozoan, which present an apolar flat geometry. By exposing T. adhaerens to a thermal gradient under a long-term imaging setup, we observe robust thermotaxis that occurs over timescale of hours, independent of any circadian rhythms. We quantify that T. adhaerens can detect thermal gradients of at least 0.1 °C/cm. Positive thermotaxis is observed for a range of baseline temperatures from 17-22.5 °C with motility trajectories to be well-described by a Levy distribution. Interestingly, the organism does not maintain a fixed orientation while performing thermotaxis. Utilizing natural diversity in size of adult organisms (100um to a few mm), we also demonstrate a critical animal size above which thermotaxis behavior is hindered. Several TRP family homologs have been previously reported to be conserved in metazoans, including in T. adhaerens. We discover naringenin, a known TRPM3 antagonist, inhibits thermotaxis in T. adhaerens . The discovery of robust thermotaxis in T. adhaerens provides a tractable handle to interrogate information processing in a brainless animal. Understanding how divergent marine animals process thermal cues is also critical due to rapid temperature rise in our oceans.

Amino acids integrate behaviors in nerveless placozoans

“…We have recorded and digitized tracks for over 2,500 animal hours of normal placozoan behavior, testing at least 50 animals for each type of behavior and using long record times of up to 24 h. This is the most comprehensive analysis of normal placozoan behaviors performed so far (see also a recent preprint by Zhong et al (2022) about a very detailed analysis of Trichoplax thermotaxis). Also, we made an effort to standardize animal conditions before testing by using only animals from the late exponential phase of culture growth.…”

Evolution of iGluR ligand specificity, polyamine regulation, and ion selectivity inferred from a placozoan Epsilon receptor

“…An interesting group of animals in the context of metazoan iGluR evolution are the early-diverging placozoans, which possess AKDF and Epsilon receptors but lack NMDA receptors present only in cnidarians and bilaterians. These animals are millimetre-sized marine invertebrates that lack synapses and a nervous system but can coordinate their cells for directed locomotive behaviors including positive and negative chemotaxis [12–15], gravitaxis [16], and thermotaxis [17]. They also elicit behavioral responses to applied substances including glycine, glutamate, GABA, protons, and synthetic regulatory peptides that mimic endogenously encoded peptides [14, 15, 18, 19].…”

Thermotaxis in an apolar, non-neuronal animal

“…Data accessibility. Descriptions of trial conditions, all centroid trajectories, analysis codes, additional analyses that did not make it into the papers, etc., are available from the GitHub repository: https:// github.com/prakashlab/Trichoplax_Thermotaxis [75].…”