Attributes of an animal's life history, such as reproductive rate or longevity, typically fall along a 'slow-fast' continuum. Animals at the fast end of this continuum, such as temperate birds, are thought to experience high rates of mortality and invest more resources in reproduction, whereas animals at the slow end, such as tropical birds, live longer, have fewer offspring and invest more resources in self-maintenance. We have previously shown that tropical birds, compared with temperate species, have a reduced basal (BMR) and peak metabolic rate (PMR), patterns consistent with a slow pace of life. Here, we elucidate a fundamental linkage between the smaller mass of central organs of tropical species and their reduced BMR, and between their smaller flight muscles and reduced PMR. Analyses of up to 408 species from the literature showed that the heart, flight muscles, liver, pancreas and kidneys were smaller in tropical species. Direct measurements on 49 species showed smaller heart, lungs, flight muscles, liver, kidneys, ovaries and testes in tropical species, as well as lower feather mass. In combination, our results indicate that the benign tropical environment imposes a relaxed selection pressure on high levels of sustained metabolic performance, permitting species to reduce the mass of organs that are energetically costly to maintain. Brain, gizzard and intestine were exceptions, even though energy turnover of brain and intestine are high. Feather mass was 37% lower in tropical species compared with similar-sized temperate birds, supporting the idea that temperate birds require more insulation for thermoregulation.