Abstract
BackgroundBones have been subjected to considerable selective pressure throughout vertebrate evolution, such as occurred during the adaptations associated with the development of powered flight. Powered flight evolved independently in two extant clades of vertebrates, birds and bats. While this trait provided advantages such as in aerial foraging habits, escape from predators or long-distance travels, it also imposed great challenges, namely in the bone structure.ResultsWe performed comparative genomic analyses of 89 bone-associated genes from 47 avian genomes (including 45 new), 39 mammalian, and 20 reptilian genomes, and demonstrate that birds, after correcting for multiple testing, have an almost two-fold increase in the number of bone-associated genes with evidence of positive selection (~52.8 %) compared with mammals (~30.3 %). Most of the positive-selected genes in birds are linked with bone regulation and remodeling and thirteen have been linked with functional pathways relevant to powered flight, including bone metabolism, bone fusion, muscle development and hyperglycemia levels. Genes encoding proteins involved in bone resorption, such as TPP1, had a high number of sites under Darwinian selection in birds.ConclusionsPatterns of positive selection observed in bird ossification genes suggest that there was a period of intense selective pressure to improve flight efficiency that was closely linked with constraints on body size.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2681-7) contains supplementary material, which is available to authorized users.
Highlights
Bones have been subjected to considerable selective pressure throughout vertebrate evolution, such as occurred during the adaptations associated with the development of powered flight
Both the avian species-tree and protein coding-genes tree showed significant differences under the tests 1sKH, SH (ShimodairaHasegawa), and expected likelihood weight (ELW) (Expected Likelihood Weight) at a critical 5 % significance level relative to those obtained with the bone-associated gene-tree-based phylogeny
Limitations imposed on body size were probably a key factor in bird evolution, as we have shown here that body mass covaried significantly with the dN/dS value only when flightless birds were included
Summary
Bones have been subjected to considerable selective pressure throughout vertebrate evolution, such as occurred during the adaptations associated with the development of powered flight. Powered flight evolved independently in two extant clades of vertebrates, birds and bats While this trait provided advantages such as in aerial foraging habits, escape from predators or long-distance travels, it imposed great challenges, namely in the bone structure. The development of pneumatic bones in birds led to reductions in overall body mass and has been associated with bone resorption [6, 9] These pneumatic bones have often been assumed to have lightened the entire avian skeleton relative to mammals [10] and to have reduced the metabolic cost of flight [3, 11,12,13,14]. Some skeletal structures, such as the humerus, ulna-radius, tibio-tarsus and fibula, have more body mass in birds than mammals [15], suggesting that modern bird skeletons have experienced diverse bone-specific selection patterns
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