Changes in Cholesterol Production Drive Tragic Octopus Death Spiral

Bimaculoid octopus. Credit: Tom Kleindinst, Marine Biology Laboratory

For all their uncanny intelligence and seemingly supernatural abilities to change color and regenerate their limbs, octopuses often suffer tragic deaths. After a mother octopus lays a clutch of eggs, she stops eating and wastes away; by the time the eggs hatch, she is dead. Some females in captivity even seem to speed up this process intentionally, mutilating themselves and twisting their arms in a tangled mess.

The source of this bizarre maternal behavior appears to be the optic gland, an organ similar to the pituitary gland in mammals. For years it was unclear how this gland triggered the horrific death spiral, but a new study by researchers from the University of Chicago, the University of Washington and the University from Illinois to Chicago (UIC) shows that the optic gland of maternal octopuses undergoes a massive change in cholesterol metabolismleading to dramatic changes in steroid hormones product. Changes in cholesterol metabolism in other animals, including humans, can have serious consequences for longevity and behavior, and the study authors believe this reveals important similarities in the functions of these steroids around the world. animal Kingdomin soft-bodied cephalopods and vertebrates.

“We know that cholesterol is important from a dietary standpoint, and in different signaling systems in the body as well,” said Z. Yan Wang, Ph.D., assistant professor of psychology and biology at the University of Washington and lead author of the study. . “It’s involved in everything from the flexibility of cell membranes to the production of stress hormones, but it was a big surprise to see it play a role in this life cycle process as well.”

Changes in Cholesterol Production Drive Tragic Octopus Death Spiral

Bimaculoid octopus. Credit: Kathryn Knight, UChicago

Self-destruct hormones

In 1977, Brandeis University psychologist Jerome Wodinsky showed that if he removed the optic gland from the Caribbean two-spotted octopus (Octopus hummelinki) mothers, they abandoned their brood, resumed feeding, and lived months longer. At the time, cephalopod biologists concluded that the optic gland must secrete some sort of “self-destructing” hormone, but what it was and how it worked was unclear.

In 2018, Wang, then a graduate student at the University of Chicago, and Clifton Ragsdale, Ph.D., professor of neurobiology at UChicago, sequenced the RNA transcriptome of the optic gland of several California two-spotted octopuses (bimaculoid octopus) at different stages of their maternal decline. RNA contains DNA’s instructions on how to make proteins, so sequencing is a good way to understand gene activity and what’s going on inside cells at any given time. As the animals began to fast and decline, there were higher levels of activity in the genes that metabolize cholesterol and produce steroids, the first time the optic gland was linked to anything other than reproduction.

In the new article, published this week in Current biology, Wang and Ragsdale took their studies a step further and analyzed the chemicals produced by the optic gland of the maternal octopus. They worked with UIC associate professor of chemistry Stephanie Cologna, Ph.D., and former UIC graduate student Melissa Pergande, who specialize in mass spectrometry, a technique that analyzes the chemical composition of samples. biological. Since Wang’s previous research showed increased activity in genes that produce steroids, they focused on cholesterol and related molecules in optic gland tissue.

Changes in Cholesterol Production Drive Tragic Octopus Death Spiral

Bimaculoid octopus. Credit: Kathryn Knight, UChicago

They found three different pathways involved in the rise in steroid hormones after breeding. One of them produces pregnenolone and progesterone, two steroids commonly associated with pregnancy. Another product of maternal cholestanoids or intermediate components for bile acidsand the third produces increased levels of 7-dehydrocholesterol (7-DHC), a precursor to cholesterol.

The new research shows that the maternal optic gland undergoes dramatic changes to produce more pregnenolone and progesterone, maternal cholestanoids and 7-DHC during decline phases. While pregnancy hormones are to be expected, this is the first time that something like the components of bile acids or cholesterol have been linked to the death spiral of the maternal octopus.

Some of these same pathways are also used to produce cholesterol in mice and other mammals. “There are two main cholesterol-creating pathways that are known from rodent studies, and now our study shows that these pathways are likely present in octopuses as well,” Wang said. “It was really exciting to see the similarity between such different animals.”

High levels of 7-DHC are toxic in humans; It’s the hallmark of a genetic condition called Smith-Lemli-Opitz Syndrome (SLOS), which is caused by a mutation in the enzyme that converts 7-DHC to cholesterol. Children with this disorder suffer severe developmental and behavioral consequences, including repetitive self-harm reminiscent of octopus end-of-life behaviors.

Changes in Cholesterol Production Drive Tragic Octopus Death Spiral

Bimaculoid octopus. Credit: Kathryn Knight, UChicago

Tiny and underrated

The results suggest that disruption of the cholesterol production process in octopuses has serious consequences, just like in other animals. So far, what Wang and his team have found is another step in the octopus’ self-destruct sequence, signaling more downstream changes that ultimately lead to the strange behavior and death of the mother.

“What’s striking is that they go through this progression of change where they seem to go crazy right before they die,” Ragsdale said. “It might be two processes, maybe three or four. Now we have at least three seemingly independent pathways to steroid hormones that could account for the multiplicity of effects these animals show.”

This summer, Wang will study at the UChicago-affiliated Marine Biological Laboratory (MBL) on the Grass Fellowship, before joining the faculty at the University of Washington. A major attraction of MBL is their extensive research program on cephalopods, in particular a new model animal, little pacific striped octopus (Ocotopus chierchiae). Among other useful characteristics like its small, manageable size, the striped octopus does not self-destruct after breeding like the animals Wang and Ragsdale have studied so far. Wang plans to examine the striped octopus’ optic glands and compare them to her new findings to look for clues as to how she avoids the octopus’ tragic death spiral.

Changes in Cholesterol Production Drive Tragic Octopus Death Spiral

Bimaculoid octopus. Credit: Kathryn Knight, UChicago

“The optic gland exists in all other soft-bodied cephalopods, and they have such divergent reproductive strategies,” she said. “It’s so small gland and that’s underappreciated, and I think it’s going to be exciting to explore how that contributes to such a wide diversity of life history trajectories in cephalopods.”

The study is titled “The Steroid Hormones of the Octopus self-destruct system.

The dark last days of an octopus mother

More information:
Z. Yan Wang, Steroid Hormones of the Octopus Self-Destruct System, Current biology (2022). DOI: 10.1016/j.cub.2022.04.043. … 0960-9822(22)00661-3

Quote: Changes in Cholesterol Production Lead to Tragic Octopus Death Spiral (May 12, 2022) Retrieved May 12, 2022 from death.html

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