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Primates of the sea

30/11/2021

Eve Seuntjens is professor in Animal Physiology and Neurobiology (Department of Biology, KU Leuven). Her research focuses on Developmental Biology. In this contribution, the octopus is the object of research.

Octopuses have fascinated people for a long time. They are often associated with nasty creatures, aliens, kraken, who have only bad intentions as they drag you into the depths. The unknown is frightening, understandable, but unjustly. Aristotle called the animals stupid creatures: “If you put your hand in the water, they will come to you”, so they are easy to catch. In the meantime, we know better. Octopuses are curious, and have a nervous system with as many neurons as a small monkey. They use their brain capacity for an extended arsenal of cognitively advanced behaviors. They can learn by observation of others, they play, they form alliances with fish to hunt efficiently. They are escape artists, they have a large memory capacity and they can dream. But these animals also acquired very special new features that we do not find in any other animals, except for other cephalopods such as cuttlefish and squid. Lightning-fast camouflage allows the octopus to go from white,  to chocolate brown. They can also change their skin texture and create bulges that resemble a plant. Their distant relatives, the cuttlefish, are absolute masters of camouflage (see video Encounter with Sepia). These color and texture changes are not only necessary for hiding in case of danger. Cephalopods use their skin as a canvas and project their emotions and intentions onto it. In this way, the skin becomes a versatile means of communication – cleverly conceived if you live underwater.


Encounter with Sepia
, Rinca, Indonesia, 2018
© video by David Moens
Sepia latimanus, when confronted with a larger organism, display a typical camouflaging behavior disguising as coral until they realise there is no threat and escape.

 

Multifunctional arms and big brains. But octopuses are anything but cruel. If you come across an octopus, you can safely extend a hand: it is sometimes answered with a careful taste contact. Indeed, octopuses taste with their suckers, which contain specialized taste receptors that direct their arms to prey. Those arms are not only used for tasting, but also for locomotion. Some octopus species have been known to use 2 arms as legs and walk around on the seabed. The other arms then serve to carry objects. The third arm from the right is different in shape in male octopuses: a hooked end can penetrate an octopus female and deposit sperm sacs. This is not yet the actual fertilization: when the female has enough eggs ready, she will choose the most suitable sperm sacs to allow her eggs to be fertilized. The latter are then neatly hung in bunches and guarded until they hatch and octopus larvae swim away (see video Dawn of a new generation). At that time, the larva of the common octopus (Octopus vulgaris) is 2 mm long, but about a quarter of its body is neural tissue (see video The unusually large octopus brain in 3D).


Dawn of a new generation 
© video by Eve Seuntjens. Leuven, Belgium, 2020
Octopus vulgaris embryos develop in egg strings during a month. At the end of development, the larval octopus uses mantle and jet muscle power to escape the egg. The birth of a new generation.

The unusually large octopus brain in 3D
© animation by Ali Murat Elagoz, imaging on a Zeiss Z1 light sheet microscope (Carl Zeiss AG, Germany), 3D reconstruction ussing ARIVIS software (Vision4D, Zeiss Edition 2.10.5), Leuven, Belgium, 2021
Light sheet microscopy imaging, brain region annotation and 3D reconstruction visualizes the space the brain occupies in a larval octopus.

 

An evolutionary enigma. The fact that octopuses have evolved within the mollusc phylum, including gastropod snails and clams, is amazing. Other than their soft bodies, these animals seem to bear very little resemblance, especially when you consider their intelligent behavior and the size of their nervous systems. How did they manage that? Research of animal evolution often uses fossils, which allows us to visualize the intermediate evolutionary steps. But how do you do that in animals that don’t have any bone in their body (besides their beak, but that alone gives little information about the shape of the body)? The development of new technologies in gene sequencing in the last 2 decades has revolutionized this. More and more genetic codes are being published for all kinds of animals, including cephalopods. We can now compare all those codes and discover which organisms are genetically more related. This has already led to the redrawing of the evolutionary tree of life, but it also led to an exciting discovery about the origin of octopuses. It relates to the order in which genes occur in the genetic material, the so-called synteny. Genetic material is organized into chromosomes, and generally, when you compare animals, gene order on chromosomes is fairly well preserved. We thus find more or less the same series of genes in all bilateria, animals with a twofold symmetry. A typical example is the Hox gene cluster, which determines the body segmentation pattern in virtually all animals, from insects to mammals.

Chromosomal big bang. Let that be just what is completely different in octopuses. While the gene sequence of the scallop and a small fish-like animal is still fairly similar, that of the octopus has been completely turned upside down. It seems that chromosomal material has been massively fragmented, then pasted back together, but differently. It’s hard to fathom how these organisms survived at all, but it’s a common feature of octopus, cuttlefish and squid genomes. We are aware of similar major changes, such as duplication of the whole genome, that is at the basis of vertebrate evolution. We know it’s rare, and it has a big impact.

But exactly what impact does such a reorganization of genes have? Thousands of genomes have been read since the Human Genome Project, which mapped the human genetic code for the first time. Scientists assumed that more complex organisms may have had many more genes than less complex creatures. However, this turned out not to be (completely) correct. The number of genes turned out to be surprisingly similar given the variety of body plans. The information in the genes therefore does not change so drastically. However, this coding information is only part of the genome. The non-coding information, which lies between the genes, contains the instructions where which gene should be transcribed, and how much of it, and for how long. If chromosomes become fragmented and linked differently, that non-coding information will also become linked to other genes. As if your stove is suddenly in the bedroom and your shower in your office. It is not inconceivable that the special appearance and new characteristics of octopuses, cuttlefish and squid could be created as a result. But it makes the fact that they were able to develop an unusually great intelligence even more special. Incomparable. Alien.


Triple heartbeat
© video by Ali Murat Elagoz, taken on a Leica DM6 upright microscope, Leuven, Belgium, 2019
An octopus has three hearts: two in the gills, and one to circulate the blood through the body. The heartbeat is already apparent in the transparent developing embryo that is growing on its yolk.

 

Eve Seuntjens