Adaptive evolution of energy metabolism genes and the origin of flight in bats

Abstract

Bat flight poses intriguing questions about how flight independently developed in mammals. Flight is among the most energyconsuming activities. Thus, we deduced that changes in energy metabolism must be a primary factor in the origin of flight in bats. The respiratory chain of the mitochondrial produces 95% of the adenosine triphosphate (ATP) needed for locomotion. Because the respiratory chain has a dual genetic foundation, with genes encoded by both the mitochondrial and nuclear genomes, we examined both genomes to gain insights into the evolution of flight within mammals. Evidence for positive selection was detected in 23.08% of the mitochondrial-encoded and 4.90% of nuclearencoded oxidative phosphorylation (OXPHOS) genes, but in only 2.25% of the nuclear-encoded nonrespiratory genes that function in mitochondria or 1.005% of other nuclear genes in bats. To address the caveat that the two available bat genomes are of only draft quality, we resequenced 77 OXPHOS genes from four species of bats. The analysis of the resequenced gene data are in agreement with our conclusion that a significantly higher proportion of genes involved in energy metabolism, compared with background genes, show evidence of adaptive evolution specific on the common ancestral bat lineage. Both mitochondrial and nuclearencoded OXPHOS genes display evidence of adaptive evolution along the common ancestral branch of bats, supporting our hypothesis that genes involved in energy metabolism were targets of natural selection and allowed adaptation to the huge change in energy demand that were required during the origin of flight.Chiroptera | genetic foundation | mitochondria | OXPHOS B ats are perhaps the most unusual and specialized of all mammals, as flight is their main mode of locomotion. Although there are several gliding mammals that are able to glide from tree to tree (such as the flying squirrel, gliding possums, and colugos), bats are the only mammal capable of sustaining level flight (1). The evolution of flight in bats was a major factor leading to the success of this amazing group (2, 3). A number of adaptations to flight found in birds are not shared by mammals, thus Darwin in the Origin of Species (Chapter 5) (4) proposed that the evolution of a flying bat from an insectivorous terrestrial mammal was too difficult to imagine.Bat flight is a highly complex functional system from a morphological, physiological, and aerodynamic perspective (5). As in birds, bat flight requires a metabolic rate that is 3-5 times greater than the maximum observed during exercise in similar-sized terrestrial mammals (2, 6). Hence, a significant metabolic barrier must separate volant from nonvolant vertebrates (6). Therefore, we speculate that energy metabolism is among the primary factors that influenced the development of flight in bats.The respiratory chain of the mitochondrial produces 95% of the adenosine triphosphate (ATP) needed for locomotion. The enzymes involved in oxidative phosphorylation (OXPHOS) are composed of multisubunit complexes that a...

Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict

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DNA sequence diversity and the efficiency of natural selection in animal mitochondrial DNA

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Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation

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