Costs and benefits of encephalization are a major topic of debate in the study of primate and human evolution. Comparative studies provide an opportunity to test the validity of a hypothesis as a general principle, rather than it being a special case in primate or hominid evolution. If a population evolves a larger brain, the metabolic costs of doing so must be paid for by either an increased energy turnover (direct metabolic constraint) or by a trade-off with other energetically expensive costs of body maintenance, locomotion, or reproduction, here referred to as the energy trade-off hypothesis, an extension of the influential Expensive Tissue Hypothesis of Aiello and Wheeler (1995, Curr. Anthropol. 36, 199-221). In the present paper, we tested these hypotheses on birds using raw species values, family means, and independent contrasts analysis to account for phylogenetic influences. First, we tested whether basal metabolic rates are correlated with brain mass or any other variable of interest. This not being the case, we examined various trade-offs between brain mass and the mass of other expensive tissues such as gut mass, which is approximated by gut length or diet quality. Only weak support was found for this original Expensive Tissue Hypothesis in birds. However, other energy allocations such as locomotor mode and reproductive strategy may also be reduced to shunt energy to an enlarged brain. We found a significantly negative correlation between brain mass and pectoral muscle mass, which averages 18% of body mass in birds and is indicative of their relative costs of flight. Reproductive costs, on the other hand, are positively correlated with brain mass in birds. An increase in brain mass may allow birds to devote more energy to reproduction, although not through an increase in their own energy budget as in mammals, but through direct provisioning of their offspring. The trade-off between locomotor costs and brain mass in birds lets us conclude that an analogous effect could have played a role in the evolution of a larger brain in human evolution.