FOSSIL BIOMOLECULES REVEAL METABOLIC AND THERMOREGULATORY STRATEGIES IN EXTINCT AMNIOTES

Birds and mammals independently evolved the highest metabolic rates among modern animals. They generate heat as a by-product of mitochondrial respiratory chain reactions. Resulting metabolic thermoregulation (endothermy) shapes the ecological niches of birds and mammals, and is considered a key advantage in their K/Pg survival and subsequent radiation.

Due to the lack of a metabolic proxy applicable to fossils, it is not known how avian and mammalian endothermy evolved. However, physiology leaves molecular signatures: Can fossil biomolecules, when analyzed in a phylogenetic framework, reveal the evolution of metabolic rates and resulting thermal strategies in extinct amniotes?

To explore molecular metabolic markers in commonly fossilized skeletal tissues, I developed a novel in situ Raman and Fourier-Transform Infrared spectroscopy protocol that allows molecular characterization of both modern and fossil samples. Non-destructive analysis (500-3000 cm^-1) of 25 extant amniote long bones demonstrated that the quantity of skeletal lipoxidation markers, byproducts of oxygen respiration, correlates (r=0.82) directly to basal metabolic rate. I assessed diagenetic alteration of this biomarker during fossilization by analyzing >40 corresponding Phanerozoic amniote bones, and showed that the signal is preserved in deep time. All fossil metabolic data were calibrated and corrected for allometry.

A time-scaled ancestral state reconstruction reveals that high metabolic rates consistent with (facultative) endothermy evolved independently in stem mammals, plesiosaurs, varanids, and the ancestral ornithodiran with an increase along the avian lineage. Avian-level metabolic rates were acquired independently on the major branches of ornithodirans. Representatives of crocodylomorphs and the major ornithischian lineages reduced their metabolic rates towards secondary ectothermy. Physiological activities of such ectotherms were strongly dependent on environmental heat and thermoregulatory behaviors, in contrast to highly active lifestyles in endothermic amniotes. Notably, widespread endothermy in many Late Cretaceous non-mammalian and non-avian amniotes suggests that features other than metabolism determined their fate during the terminal Cretaceous mass extinction.