Estimates of Positive Darwinian Selection Are Inflated by Errors in Sequencing, Annotation, and Alignment

Schneider, Adrian; Souvorov, Alexander; Sabath, Niv; Landan, Giddy; Gonnet, Gastón H.; Graur, Dan

doi:10.1093/gbe/evp012

Cited by 103 publications

(107 citation statements)

References 23 publications

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“…This observation supports our hypothesis that energy metabolism played a crucial role in the attainment of flight by bats. A caveat of our genome-wide analyses is that both of the bat genomes (little brown bat and flying fox) used to identify nuclear-encoded OXPHOS and mitochondrial protein genes are only of draft quality (1.7× and 2.63×, respectively); thus, a smaller number of complete genes could be identified and analyzed, and required additional care to avoid false-positive predictions (36). To control for the quality of the gene data in the analyses of the nuclear-encoded OXPHOS genes and mitochondrial protein genes, we used two approaches (i): measurement of the background rate of positive selection in the draft bat genomes, and (ii) resequencing of OXPHOS genes from several bat species and reanalysis.…”

Section: Resultsmentioning

confidence: 99%

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

Shen

Lü

Zhu

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

247

218

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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...

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Section: Resultsmentioning

confidence: 99%

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

Shen

Lü

Zhu

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

247

218

View full text Add to dashboard Cite

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“…Alignment quality is of major importance for ω estimation because errors can lead to the misidentification of synonymous sites as nonsynonymous sites 37 . To minimize the effect of alignment errors, two algorithms, SATé-II and DIALIGN-TX 38 , were chosen to align each ortholog, as they have been reported to be robust in dealing with global and local alignments, respectively (Supplementary Note).…”

Section: Genome Evolution Analysismentioning

confidence: 99%

Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle

et al. 2013

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6 3 l e t t e r sAs top predators, falcons possess unique morphological, physiological and behavioral adaptations that allow them to be successful hunters: for example, the peregrine is renowned as the world's fastest animal. To examine the evolutionary basis of predatory adaptations, we sequenced the genomes of both the peregrine (Falco peregrinus) and saker falcon (Falco cherrug), and we present parallel, genome-wide evidence for evolutionary innovation and selection for a predatory lifestyle. The genomes, assembled using Illumina deep sequencing with greater than 100-fold coverage, are both approximately 1.2 Gb in length, with transcriptome-assisted prediction of approximately 16,200 genes for both species. Analysis of 8,424 orthologs in both falcons, chicken, zebra finch and turkey identified consistent evidence for genome-wide rapid evolution in these raptors. SNP-based inference showed contrasting recent demographic trajectories for the two falcons, and gene-based analysis highlighted falcon-specific evolutionary novelties for beak development and olfaction and specifically for homeostasisrelated genes in the arid environment-adapted saker.

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“…We used Spearman's rank correlation to determine if the following characteristics of the sequence data were correlated with the P values from the LRTs: (i) average GC content at the third position; (ii) average overall GC content; (iii) transition/transversion ratio (kappa); and (iv) d N tree length. The gappiness of an alignment could introduce potential biases in our results (17,18), so we also looked for correlations between the P values from the LRTs and two metrics to assess coverage in our alignments: (i) gap percent (gapPCT), or the sum of the number of gaps in each sequence in an alignment divided by the sum of the total number of sites in all of the sequences in an alignment; and (ii) an alignment quality score (described in SI Text). Only a few of these characteristics of the data were significantly correlated (P < 0.05) with the P values of the LRTs, but all correlations were very weak (range of Spearman's rho = −0.1-0.06, for all tests; Dataset S2).…”

Section: Heterogeneous Patterns Of Molecular Evolution Among Bee Linementioning

confidence: 99%

Genes involved in convergent evolution of eusociality in bees

Woodard

Fischman

Venkat³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

197

225

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Eusociality has arisen independently at least 11 times in insects. Despite this convergence, there are striking differences among eusocial lifestyles, ranging from species living in small colonies with overt conflict over reproduction to species in which colonies contain hundreds of thousands of highly specialized sterile workers produced by one or a few queens. Although the evolution of eusociality has been intensively studied, the genetic changes involved in the evolution of eusociality are relatively unknown. We examined patterns of molecular evolution across three independent origins of eusociality by sequencing transcriptomes of nine socially diverse bee species and combining these data with genome sequence from the honey bee Apis mellifera to generate orthologous sequence alignments for 3,647 genes. We found a shared set of 212 genes with a molecular signature of accelerated evolution across all eusocial lineages studied, as well as unique sets of 173 and 218 genes with a signature of accelerated evolution specific to either highly or primitively eusocial lineages, respectively. These results demonstrate that convergent evolution can involve a mosaic pattern of molecular changes in both shared and lineage-specific sets of genes. Genes involved in signal transduction, gland development, and carbohydrate metabolism are among the most prominent rapidly evolving genes in eusocial lineages. These findings provide a starting point for linking specific genetic changes to the evolution of eusociality. social evolution | social insects | sociogenomics | molecular phylogenetics

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Estimates of Positive Darwinian Selection Are Inflated by Errors in Sequencing, Annotation, and Alignment

Cited by 103 publications

References 23 publications

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

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

Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle

Genes involved in convergent evolution of eusociality in bees

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