Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur

Abstract

Birds and mammals independently evolved the highest metabolic rates among living animals. Their metabolism generates heat that enables active thermoregulation, shaping the ecological niches they can occupy and their adaptability to environmental change. The metabolic performance of birds, which exceeds that of mammals, is thought to have evolved along their stem lineage. However, there is no proxy that enables the direct reconstruction of metabolic rates from fossils. Here we use in situ Raman and Fourier-transform infrared spectroscopy to quantify the in vivo accumulation of metabolic lipoxidation signals in modern and fossil amniote bones. We observe no correlation between atmospheric oxygen concentrations and metabolic rates. Inferred ancestral states reveal that the metabolic rates consistent with endothermy evolved independently in mammals and plesiosaurs, and are ancestral to ornithodirans, with increasing rates along the avian lineage. High metabolic rates were acquired in pterosaurs, ornithischians, sauropods and theropods well before the advent of energetically costly adaptations, such as flight in birds. Although they had higher metabolic rates ancestrally, ornithischians reduced their metabolic abilities towards ectothermy. The physiological activities of such ectotherms were dependent on environmental and behavioural thermoregulation, in contrast to the active lifestyles of endotherms1. Giant sauropods and theropods were not gigantothermic, but true endotherms. Endothermy in many Late Cretaceous taxa, in addition to crown mammals and birds, suggests that attributes other than metabolism determined their fate during the terminal Cretaceous mass extinction.