Inside Out: How sexual dimorphism and neural plasticity shape the brain, behaviour, and longevity in octopuses

HSF 25116 | Amount: $87,000 | Project Leader: W Chung | Project Period: 3 yrs

A project undertaken at the University of Queensland, and supervised by Wen-Sung Chung

Sexual dimorphism is common in animals where females and males differ in body size, sex-dependent characteristics, behaviour and life history. Behavioural sexual dimorphisms, like courtship display or parental care, are often influenced by differences in the nervous system. For animals with large and complex brains, these differences have been assessed in detail in mammals and birds. However, little is known about sexual dimorphism in large-brained invertebrates.

Octopuses diverged from vertebrates approximately 500 million years ago. Octopuses can solve complex tasks, learn new tricks through observation, and show distinct sexual dimorphisms in body anatomy and mating behaviours, similar to mammals. However, their molluscan brain lacks a somatotopic neural layout, making it utterly different to vertebrates. The ability of octopuses to rapidly solve complex tasks using a sophisticated yet different brain challenges our knowledge of animal cognition. This raises the question of how different brain Bauplan can lead to similar cognitive outputs. Another difference is that octopuses only live for one year, and as their brains expand over 5,000 times, they show distinct sexual differences in morphology and behaviour. Remarkably, octopuses die after a single mating event without passing on their life-long experiences to their offspring. Considering the high metabolic costs involved in growth and learning to then ‘waste’ the acquired knowledge, it remains a mystery why octopuses evolved such elaborate brains in the first place, and how they evolved in these super-smart snails remains a mystery. Hence, more thoroughly studied vertebrate models should be compared to the phylogenetically distinct octopuses to reveal whether common developmental principles govern the evolution of large complex brains in all animals.

This project aims to provide a modern neuroscience foundation to map the ontogenetic plasticity of the octopus brain. Using a multidisciplinary approach, we aim to investigate rapid fluctuations in octopus brain size, differentiation of underlying neural networks and their function during growth and reproduction.

The blue-lined octopus, Hapalochlaena fasciata, fulfils key criteria for use as a model:

1) It is an iconic Australian native species, and wild specimens can readily be collected all year round from coastal habitats;

2) it is one of very few octopus species for which the life cycle can be closed in captivity, which offers an opportunity to study its entire lifespan and the associated brain plasticity;

3) our discovery of a distinct sexual dimorphism in brain development leading to differences in the timing of male and female deaths is in stark contrast to traditional neuroscience model systems such as nematodes, flies, rodents and humans.

This work will uncover the principles of complex invertebrate neuroarchitecture, function, and behaviours between sexes. Once we understand how the octopus brain is remodelled during development, we can compare the processes that lead to the emergence of large-brained species across the animal kingdom. The expected outcomes promise to answer long-standing questions about brain plasticity and longevity in all animals, which may not be achieved by studying traditional ‘smart’ complex-brained model vertebrates.