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Flight demand and environmental niche are associated with molecular evolutionary rates in a large avian radiation

Among the macroevolutionary drivers of molecular evolutionary rates, metabolic demands and environmental energy have been a central topic of discussion. The large number of studies examining these associations have found mixed results, and have rarely explored the interactions among various factors impacting molecular evolutionary rates. Taking the diverse avian family Furnariidae as a case study, we examined the association between several estimates of molecular evolutionary rates with proxies of metabolic demands imposed by flight (wing loading and the hand-wing index) and proxies of environmental energy across the geographic ranges of species (temperature and UV radiation). We found evidence that species that fly less have greater wing loading and this is associated with accelerated rates of mutation. An elongated wing morphology is associated with greater flight activity and with molecular signatures of positive selection or reduced population sizes. Meanwhile, environmental temperature and UV radiation interact to explain molecular rates at sites affected by selection and population size, contrary to the expectation of their impact on mutation rates. Our results suggest that the demands of flight and environmental energy pose multiple evolutionary pressures on the genome either by driving mutation rates or via their association with natural selection or population size.