Long after its ancestors erased its genetic code for hard armor, a marine octopus has reinvented a recipe for making a shell.
A recent genetic analysis of the paper nautilus or greater argonaut (Argonauta argo) has revealed a surprising origin for its protective shell, which is unlike the shell of its closest relatives.
Instead of wearing their shells outside like sensitive snails, most cephalopods (which are also molluscs) have shed their hard outer shell. Many, such as octopuses and squids, have lost their shells entirely or only vestigial remains remain.
Others, such as the cuttlefish and the ram’s horn squid (Spirula spirula), carry the shell inside. The ram’s horn squid has a spiral shell with an internal chamber that acts as a kind of skeleton. Buoyant and surprisingly durable, it is often washed up on beaches.
A rare exception among cephalopods is the nautilus (Nautilus belauensis), which still has an outer shell, complete with air chambers that it uses to regulate its buoyancy as it floats across the open oceans. Their shells, and those of now-extinct cephalopod ancestors, are made of proteins that incorporate minerals such as aragonite and calcite into intricate microscopic structures.
Originating sometime in the Ordovician period, at least 440 million years ago, the ancestors of all modern cephalopods are thought to have had these protective structures.
Although commonly known as a paper nautilus, argonauts are actually a genus of octopus. In this unusual group, only females produce a protective spiral shell, by secreting calcifying proteins from their arms. Argonauts wear these shells externally like a nautilus, and their shapes are almost identical, but this shell has a completely different microscopic structure.
Also, instead of being attached to their mantle, Argonauts are attached to their shell houses by several of their arms.
Shells of the six species of argonauts still alive. (Mgiganteus1/Wikimedia commons/CC BY-SA 3.0)
Since most octopuses lost their outer gut long ago, researchers have wondered how and why only one group regained a shell.
Working with a team of researchers from across Japan, marine biologist Masa-aki Yoshida of Shimane University sequenced the DNA of Argonauta argo. They compared the genome of argonauts to other molluscs, including the California two-spotted octopus (Octopus bimaculoides) and the nautilus.
“Consistent with the above results, most of the proteins are apparently not shared with shell matrix proteins [cephalopods and relatives]including those of Nautilus,” the team writes in their paper.
Some of the genes and the proteins they express, however, have been found in other shelled molluscs such as the clam (Lottia gigantea) and the Japanese pearl oyster (Pinctada fucata). Other sequences were found in shellless octopuses, suggesting that the argonaut repaired its protective shell using proteins unrelated to ancestral shell formation.
Unlike other octopuses, argonauts are not benthic: they do not live near the sea floor or other structures. Instead, they have taken up the life of vagabonds, floating in the middle of the tropical and subtropical open seas all their lives. This is the same pelagic lifestyle that the nautilus shares.
To achieve this, the Argonauts needed techniques to enable easy flotation as well, Yoshida and the team explain. Although its shell lacks the more complicated internal structure of nautilus air chambers, it can still trap some air.
This shell is also known to be the argonaut’s egg, which would explain why only females develop them. Females cover their eggs within the protection of the shell, eliminating the need to hide the eggs in a substrate such as the sea floor as most other octopuses do.
Argonauts seem to have completely reinvented the shell from scratch to help it transition from substrate dweller to water drifter, mimicking the nautilus in a remarkable example of convergent evolution.
This research was published in Genome Biology and Evolution.