Evolutionary and developmental implications of enhanced encephalization

The development of an enlarged and elaborated brain is considered a defining characteristic of human evolution1. The evolution of the Homo clade has been accompanied by significant encephalization2,3. This facilitated the development of more complex social strategies4,5, more effective food acquisition6 and the ability to solve ecological problems through innovative means7. Each of these characteristics may have increased survival and reproductive success, giving a greater life expectancy at the age of first reproduction8.

While the benefits of encephalization are numerous, the brain imposes significant metabolic costs on both the individual9,10,11. High levels of energetic expenditure are necessitated by the brain’s responsibility for regulating the body’s energy supply and controlling the function of many peripheral organs12. These functions require intense neuronal activity, giving the brain the highest metabolic demand relative to size of all organs13.

The question of how larger brains can be metabolically afforded has remained a prominent problem in human evolution11,14,15,16,17. Life history theory states that as energy availability is finite, an organism has a limited energy budget. Energy allocated to one function cannot be used for another. Energy savings in other organs or tissues could allow for energetic diversion to the brain, without the need to increase overall metabolic expenditure11,18. Such a trade-off has been proposed with both digestive tract development17 and adiposity19.

Meeting the brain’s metabolic requirements

The immediate metabolic costs of the brain depend on its activation state. While the metabolic rate is low during sleep20 increased energy consumption has been observed in response to a mental task21, and following somatosensory, olfactory, visual and auditory stimulation22,23,24,25,26,27. The adult brain almost exclusively derives its energy from the metabolism of glucose28. This, coupled with its high energetic demand, ensure that the brain metabolises the most glucose of any organ29,30. The brain, however, is unable to store significant amounts of energy and hence buffer its high yet variable metabolic demand31. As such, the body is required to supply glucose to the brain quickly and effectively. The ‘Selfish Brain Hypothesis’12 posits that the brain prioritises its own glucose needs over those of the peripheral organs, such as skeletal muscle.

Skeletal muscle and encephalization

Skeletal muscle mass is an expensive tissue to maintain, accounting for approximately 20% of human male BMR32,33, and may be compromised to partially offset the brain’s high energy costs11,34. An adaptation to reduce muscle mass would thereby reduce metabolic demand, allowing for a reallocation of energy towards the central nervous system35. The glucose demands of skeletal muscle also increase significantly with activation36,37,38,39,40. In such circumstances, skeletal muscle thereby becomes a powerful competitor of the brain for glucose and oxygen41.

High intensity exercise increases the metabolic demand of skeletal muscles and the brain39,40,42,43,44,45, in proportion to degree of activation. At high levels of activation both are reliant upon glucose metabolism, and require a high rate of oxygen and glucose supply. Should both be challenged simultaneously, competition for these valuable yet limited resources may therefore develop, with one or both organs receiving an insufficient supply for optimal performance.

The concept of an antagonistic relationship between capacity to perform mental and physical work is not a new one46. As described by the idea of central fatigue, prior mental exertion may impair subsequent physical performance47.

Despite the intuitive appeal of a trade-off between two competing functions, negative covariance in such traits are not frequently observed when phenotypic comparisons are made between individuals within a population48,49. This study seeks to experimentally investigate the possibility of a trade-off involving the brain at the acute, rather than at the evolutionary or developmental, level. It is hypothesised that, when both systems are challenged simultaneously, performance will be inferior to performance when each are challenged in isolation. It is further hypothesised that the relative decrease in muscle power output will exceed the relative decrease in cognitive function.