Studies reveal how octopuses evolved to sense their surroundings over 300 million years

“They use their arms for ‘taste by touch’ contact-dependent aquatic exploration of crevices in the sea floor,” said senior investigator Nicholas Bellono, associate professor in the Department of Molecular and Cellular Biology at Harvard.

The second paper takes a look at how these chemical receptors arose in cephalopods, such as squids. Using a combination of genetic profiling, physiology, and behavioral analyses, the team found that squid receptors have adapted over time to sense bitter molecules in their surroundings. So if a squid senses bitterness in a molecule, it will interpret it as a toxic or undesirable entity and will release it.

Bellono, who was a co-author in the second paper as well, explains, “In this case, there were fewer receptors than in the octopus, and they looked more like the neurotransmitter binding pocket in that it can bind more hydrophilic molecules. We see this difference between the octopus and squid as reflecting an evolutionary timeline and adaptation, where we see the transition from neurotransmission in acetylcholine receptors to soluble bitter taste in the squid, to the most recent innovation of taste-by-touch sensing of insoluble molecules in octopus.”

This analysis of cephalopod genomes has shown that even though squids and octopuses come from the same ancestor, their sensory receptors have evolved independently after an evolutionary split some 300 million years ago.

Study abstract 1

Chemotactile receptors (CRs) are a cephalopod-specific innovation that allow octopuses to explore the seafloor via ‘taste by touch’1. CRs diverged from nicotinic acetylcholine receptors to mediate contact-dependent chemosensation of insoluble molecules that do not readily diffuse in marine environments. Here we exploit octopus CRs to probe the structural basis of sensory receptor evolution. We present the cryo-electron microscopy structure of an octopus CR and compare it with nicotinic receptors to determine features that enable environmental sensation versus neurotransmission. Evolutionary, structural and biophysical analyses show that the channel architecture involved in cation permeation and signal transduction is conserved. By contrast, the orthosteric ligand-binding site is subject to diversifying selection, thereby mediating the detection of new molecules. Serendipitous findings in the cryo-electron microscopy structure reveal that the octopus CR ligand-binding pocket is exceptionally hydrophobic, enabling sensation of greasy compounds versus the small polar molecules detected by canonical neurotransmitter receptors. These discoveries provide a structural framework for understanding connections between evolutionary adaptations at the atomic level and the emergence of new organismal behaviour.

Study abstract 2

The evolution of new traits enables expansion into new ecological and behavioural niches. Nonetheless, demonstrated connections between divergence in protein structure, function and lineage-specific behaviours remain rare. Here we show that both octopus and squid use cephalopod-specific chemotactile receptors (CRs) to sense their respective marine environments, but structural adaptations in these receptors support the sensation of specific molecules suited to distinct physiological roles. We find that squid express ancient CRs that more closely resemble related nicotinic acetylcholine receptors, whereas octopuses exhibit a more recent expansion in CRs consistent with their elaborated ‘taste by touch’ sensory system. Using a combination of genetic profiling, physiology and behavioural analyses, we identify the founding member of squid CRs that detects soluble bitter molecules that are relevant in ambush predation. We present the cryo-electron microscopy structure of a squid CR and compare this with octopus CRs1 and nicotinic receptors2. These analyses demonstrate an evolutionary transition from an ancestral aromatic ‘cage’ that coordinates soluble neurotransmitters or tastants to a more recent octopus CR hydrophobic binding pocket that traps insoluble molecules to mediate contact-dependent chemosensation. Thus, our study provides a foundation for understanding how adaptation of protein structure drives the diversification of organismal traits and behaviour.