Maternal Octopus Suicide: Transcriptome changes in mother octopi brain cause them to kill themselves during the brooding process

Disclaimer: This blog post has been adapted from an essay I wrote in my neuroethology class. The students 邱筠筑,  莊逸琪, and  文馨瑩 gave the lecture on the paper: Multiple optic gland signaling pathways implicated in octopus maternal behavior and death. The paper was written by professors, Z. Yan Wang and Clifton W. Ragsdale


Octopi are one of the most intelligent invertebrates in the animal kingdom, and thus their radically different brain and mating cycle is of keen interest to researchers. One peculiar aspect of the octopus is its mating cycle; octopi are known to eat one another, and especially like to eat younger octopi. Unfortunately, mother octopi cannot distinguish between their young, and other random octopi. In a cruel twist of fate, evolution solved this problem by having the mother die soon after birth. Sadly for the mother octopus, this process is a slow 4 to 8 week deterioration, where the octopus stops eating, and engages in suicidal self harm. Eventually, the octopus will pass, and the next generation of octopi is born.

The octopus mating cycle is orchestrated by the optic gland, which much like its namesake, is located near the optic lobe. This gland is much like the pituitary gland in humans, and orchestrates the reproductive cycle in octopi. Here, the olfactory lobe has an excitatory effect on the optic gland while the Subpedunculate lobe has an inhibitory effect. The Subpedunculate lobe uses FMRMamide to inhibit the optic gland To confirm the optical glands role in the maternal degeneration, Wodinsky et al. removed the optic gland after laying the eggs. The octopi, had no idea they had given birth, and did not degenerate, returning to normal feeding patterns associated with virgin octopi.

Here the authors wanted to know what changes occured in the optical gland transcriptome and ideally looked to glean information on the effects of these changes on the behavior. Here, a transcriptome measures the increase in tRNA that signals that these particular proteins are being synthesized, and thus can be tied to an increase (or decrease) in particular biochemical processes like neuropeptide or steroid production. By breaking the octopus brooding cycle down into four stages, and determining the transcriptomes at each stage, the scientists are able to correlate behavior and biochemical processes.

During the experimental process they determined 4 stages, the non-mated stage, the feeding stage (have mated, but still eat), the fasting stage (no longer eat), and the decline stage (with self-harm behavior). Each stage appears to be non-reversible, with no octopi moving backwards in the progression. They perform the transcriptome analysis, and identify three unique clusters of genes that show changes over the course of the brooding period. There are three clusters identified. Cluster one is increased from non-mating to feeding stage, Cluster two is increased from feeding to fasting, And cluster three shows a decrease from non-mating to feeding.

Cluster-one and Cluster-three are both related to the transition from non-mated to feeding. This is the first key transition after sex. There seems to be an increase in genes related to neurotransmission and biosynthesis. Specifically, many genes associated with exocytosis of synaptic vesicles seems to be upregulated including synaptotagmin, as well as many receptors including acetylcholine, and octopamine. Furthermore there is an increase in genes associated with steroid production. This is not surprising given that neural transmission should be going up in a region associated with mating behavior. Interesting, cluster-three shows  a large portion of genes related to feeding behavior get downregulated during this period as well.  Specifically the feeding circuit activating peptide and FMRFamide peptide are down regulated. Recall FMRFamide is instrumental in inhibiting the optical gland. Obviously this helps to explain the lack of feeding in octopi. Also, there is a downregulation in dopamine as well. This could potentially explain the self harm near the end of the life cycle, but that is only a hypothesis.

As mentioned, cluster-two shows activation when the octopus switches from the feeding to the fasting state. The most interesting increase is that of Insulin growth factor protein ImpL2 is upregulated. This results in an increased tissue degradation. This peptide results in insulin being less effective effectively starving the cells, and ushering in the death of the mother octopus.

While transcriptome analysis is only corrilational it does give scientists many new pathways to test in the lab, and many of these pathways could be integral in the death of maternal octopi. Furthermore, it provides further evidence that FMRFamide is key in inhibiting the optical glands. To conclude,  transcriptome analysis is not sufficient it is a useful tool in probing neurobiology of octopi’s reproductive cycle.


Author: Alex White
Acknowledgements:  邱筠筑  莊逸琪, and  文馨瑩


Source:Multiple optic gland signaling pathways implicated in octopus maternal behavior and death Z. Yan Wang and Clifton W. Ragsdale

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