Octopus and cuttlefish suckers may have evolved by repurposing ancient developmental genes

Cephalopods, like the octopus, have specialized arms and suckers, but how these structures evolved from the simple bodies of their mollusk ancestors remains a mystery. Researchers from the University of Tokyo compared gene activity during embryonic development of cuttlefish, octopus and snail body parts. They found that several genes associated with appendage patterning showed expression along developing cephalopod arms, but no comparable patterns in developing suckers. Developing suckers instead expressed Ets1, a gene associated with early embryonic development in mollusks. The findings suggest cephalopods evolved suckers by reusing existing genes in new ways.

Squids, octopuses, cuttlefish and enigmatic nautiluses are creatures that intrigue anyone with an affinity for sea life. They have many distinctive features, including long prehensile arms with suckers for gripping prey. That they share a common ancestor with gastropods such as slugs and snails can be surprising to some, given how the former are famed for their intelligence and complex behavior, while the latter are not. But this raises the question: How did cephalopods' complex arms with functional suckers evolve from the simple foot of a mollusk ancestor?

The work is published in the journal iScience.

Arm and sucker development diverge

"Our findings suggest that cephalopod arm development involves conserved patterning genes also used in appendage development in other animals like insects and mammals. But suckers on their arms have a unique developmental mechanism in which a gene used in early embryogenesis, Ets1, is reused," said postdoctoral fellow Ryosuke Kimbara.

"At first, we hypothesized that appendage patterning genes would be involved both in arm and sucker patterning. But we ran into a challenge in identifying the genes expressed in suckers. Therefore, we switched to a more comprehensive method and continued screening until we found a gene with a distinctive expression pattern in developing suckers, and it wasn't where we expected to find it."

An embryonic gene resurfaces in suckers

While looking at potential genetic explanations for sucker development, one gene, Ets1, which is normally involved in early developmental processes in mollusks, stood out. The researchers found Ets1 activity in the region where suckers form in cuttlefish and octopus. They also noticed changes in cell shapes and the way cells moved as suckers developed, processes that resemble those during a developmental process called epithelial-mesenchymal transition, or EMT. These findings suggest genes involved in early embryonic development may have been reused later in development to help build the specialized structure of a sucker.

However, the researchers stress that the precise role of Ets1 and the extent to which EMT is involved still need to be experimentally tested.

"In suckers, cell activities like changes in shape, movement and cell proliferation will be involved in the morphological changes that create the adhesive structure," said Kimbara. "Since these processes are similar to those observed in early embryonic development, it is assumed that the shared mechanism would be recruited to sucker production even in later developmental stages.

"Also, although the developmental process and gene expression pattern of suckers at the early developmental stages are very similar between cephalopods, such as squid and cuttlefish, and octopus, their developed sucker morphology and adhesive mechanism are different. Therefore, during the acquisition process of sucker structures in each lineage, the underlying molecular mechanism may also have evolved independently."

Gene reuse needs experimental confirmation

These findings are important for showing how evolution can produce new structures without necessarily requiring entirely new genes. Instead, genes that already have important roles elsewhere in the body can be co-opted for novel purposes. The researchers say that similar gene-reuse mechanisms may eventually help explain other unusual cephalopod structures, including chromatophores (pigment cells), the ink sac and the hard beak, although more research is needed.

They also emphasize that the current study mainly identifies patterns of gene activity rather than directly testing what each gene does. Experiments that switch individual genes on or off, together with comparisons across more mollusk species, will be needed to find out how these genes actually contribute to sucker formation and how this distinctive structure evolved.