The capacity for flight is frequently associated with greater species longevity, such as in bats, for example. The present consensus suggests that the cellular adaptations needed to support the greater metabolic capacity required for flight also resist some forms of molecular damage important in aging. This is particularly the case for adaptations in mitochondria, the power plants of cells, where damage and loss of function is known to be important in aging. The membrane pacemaker hypothesis is one way of looking at this; species that evolve cell membranes that are more resilient to oxidative damage will live longer as a result.
Today’s open access paper reports on the interesting approach of using gain and loss of flight in evolutionary history as a way to look for genes and functions that might be important in aging. It is a good idea, but unfortunately didn’t pan out in this particular study – commonalities between species were lacking. That a modest selection of species failed to produce shared genetic adaptations that appear relevant to aging and longevity may indicate the existence of broad a diversity of mechanisms relevant to metabolism and flight, rather than just a few important mechanisms, or perhaps a very complex, multifaceted relationship between metabolism and longevity. Other lines of work, such as the so far largely unsuccessful search for longevity-related genes with meaningful effect sizes in humans, support the latter conjecture.
Maximum life span (MLS) is a fundamental life-history trait related to the rate of aging and senescence in animals. It has been proposed that species with lower extrinsic mortalities have longer life spans because they can invest in long-term survival. Extrinsic mortality is generally determined by ecological factors, such as climate and predation risk, and may drive shortened or extended life spans through natural selection. However, MLS is influenced by complex molecular and metabolic processes such as mitochondrial homeostasis.
Mitochondria of aerobic animals produce reactive oxygen species (ROS), which can damage lipids, proteins, and nucleic acids. A low rate of mitochondrial ROS generation reportedly leads to long life spans in both long-lived and calorie-restricted animals because of low levels of both oxidative stress and accumulation of mutations in somatic mitochondrial DNA. Because animals with higher metabolic rates produce more ROS, a causal relationship between metabolic rate and life span can be expected. Additionally, a positive relationship between body mass and life span is pervasive in vertebrates. Because metabolic rates per mass are lower with increasing body mass, animals with smaller body masses could suffer more from ROS, and their life spans would be correspondingly shorter.
However, flight ability significantly affects MLS and aging rates in both mammals and birds regardless of body mass. Flight typically requires higher rates of energy consumption and generates more ROS than other types of locomotion, such as walking or swimming. However, a prolonged life span often evolved with the acquisition of flight ability, suggesting that there is no simple relationship between metabolism and life span.
Here, we examine the parallel evolution of flight in mammals and birds and investigate positively selected genes at branches where either the acquisition (in little brown bats and large flying foxes) or loss (in Adélie penguins, emperor penguins, common ostriches, emus, great spotted kiwis, little spotted kiwis, okarito brown kiwis, greater rheas, lesser rheas, and cassowaries) of flight abilities occurred. Although we found no shared genes under selection among all the branches of interest, 7 genes were found to be positively selected in 2 of the branches. Among the 7 genes, only IGF2BP2 is known to affect both life span and energy expenditure. The positively selected mutations detected in IGF2BP2 likely affected the functionality of the encoded protein. IGF2BP2, which has been reported to simultaneously prolong life span and increase energy expenditure, could be responsible for the evolution of shortened MLS associated with the loss of flying ability.