Base Compositional Bias and Phylogenetic Analyses: A Test of the “Flying DNA” Hypothesis

Bussche, Ronald A. Van Den; Baker, Robert J.; Huelsenbeck, John P.; Hillis, David M.

doi:10.1006/mpev.1998.0531

Cited by 46 publications

(22 citation statements)

References 51 publications

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“…Previous studies suggested that bats have "flying DNA," DNA that is composed of elevated levels of adenine and thymine (37); therefore, we tested the bias of base frequencies and codon usage for the genes that we studies. Consistent with a previous study (38), we failed to find the common trend of elevated levels of adenine and thymine or codon bias for bats (data available upon request). Thus, our observation of elevated levels of positive selection for OXPHOS related genes is not simply due to changes in base frequency or codon bias in bats.…”

Section: Resultssupporting

confidence: 90%

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.

254

225

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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: Resultssupporting

confidence: 90%

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.

254

225

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“…Pettigrew's flying primate hypothesis stimulated a gestalt of scientific studies aimed at examining the question of chiropteran monophyly (1). Both hard-and soft-character morphological studies and molecular studies unanimously support the monophyly of Chiroptera (3,5,10,12,31,44).…”

Section: Monte Carlo Simulationsmentioning

confidence: 95%

“…Pettigrew and colleagues (1,2) challenged the systematics community with the ''flying primate hypothesis,'' which associates megabats with primates and dermopterans rather than with microbats. Recent morphological and molecular studies disagree with Pettigrew's hypothesis and support traditional bat monophyly (3)(4)(5). At the interordinal level, the conventional view based on morphology is that bats group in Archonta with dermopterans, primates, and scandentians (6,7).…”

mentioning

confidence: 88%

Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats

Teeling

Madsen

Bussche

et al. 2002

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

Self Cite

181

114

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Molecular phylogenies challenge the view that bats belong to the superordinal group Archonta, which also includes primates, tree shrews, and flying lemurs. Some molecular studies also challenge microbat monophyly and instead support an alliance between megabats and representative rhinolophoid microbats from the families Rhinolophidae (horseshoe bats, Old World leaf-nosed bats) and Megadermatidae (false vampire bats). Another molecular study ostensibly contradicts these results and supports traditional microbat monophyly, inclusive of representative rhinolophoids from the family Nycteridae (slit-faced bats). Resolution of the microbat paraphyly͞monophyly issue is essential for reconstructing the temporal sequence and deployment of morphological character state changes associated with flight and echolocation in bats. If microbats are paraphyletic, then laryngeal echolocation either evolved more than once in different microbats or was lost in megabats after evolving in the ancestor of all living bats. To examine these issues, we used a 7.1-kb nuclear data set for nine outgroups and twenty bats, including representatives of all rhinolophoid families. Phylogenetic analyses and statistical tests rejected both Archonta and microbat monophyly. Instead, bats are in the superorder Laurasiatheria and microbats are paraphyletic. Further, the superfamily Rhinolophoidea is polyphyletic. The rhinolophoid families Rhinolophidae and Megadermatidae belong to the suborder Yinpterochiroptera along with rhinopomatids and megabats. The rhinolophoid family Nycteridae belongs to the suborder Yangochiroptera along with vespertilionoids, noctilionoids, and emballonuroids. These results resolve the apparent conflict between previous molecular studies that sampled different rhinolophoid families. An important implication of rhinolophoid polyphyly is independent evolution of key anatomical innovations associated with the nasal-emission of echolocation pulses.bats ͉ Chiroptera ͉ echolocation ͉ Mammalia ͉ phylogeny

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“…Pettigrew (1994) suggested that flying vertebrates should have elevated levels of A and T nucleotides because of higher metabolic demands. However, analysis by Van Den Bussche et al (1998) showed that flying mammals such as bats do not have higher AT levels than other mammals. Our results suggest that birds also may not show the elevated AT levels predicted by Pettigrew (1994).…”

Section: Genome Research 619mentioning

confidence: 98%

MHC Class II Pseudogene and Genomic Signature of a 32-kb Cosmid in the House Finch (Carpodacus mexicanus)

Hess¹,

Gasper²,

Hoekstra³

et al. 2000

Genome Res.

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Large-scale sequencing studies in vertebrates have thus far focused primarily on the genomes of a few model organisms. Birds are of interest to genomics because of their much smaller and highly streamlined genomes compared to mammals. However, large-scale genetic work has been confined almost exclusively to the chicken; we know little about general aspects of genomes in nongame birds. This study examines the organization of a genomic region containing an Mhc class II B gene in a representative of another important lineage of the avian tree, the songbirds (Passeriformes). We used a shotgun sequencing approach to determine the sequence of a 32-kb cosmid insert containing a strongly hybridizing Mhc fragment from house finches (Carpodacus mexicanus). There were a total of three genes found on the cosmid clone, about the gene density expected for the mammalian Mhc: a class II Mhc ␤-chain gene (Came-DAB1), a serine-threonine kinase, and a zinc finger motif. Frameshift mutations in both the second and third exons of Came-DAB1 and the unalignability of the gene after the third exon suggest that it is a nonfunctional pseudogene. In addition, the identifiable introns of Came-DAB1 are more than twice as large as those of chickens. Nucleotide diversity in the peptide-binding region of Came-DAB1 (⌸ = 0.03) was much lower than polymorphic chicken and other functional Mhc genes but higher than the expected diversity for a neutral locus in birds, perhaps because of hitchhiking on a selected Mhc locus close by. The serine-threonine kinase gene is likely functional, whereas the zinc finger motif is likely nonfunctional. A paucity of long simple-sequence repeats and retroelements is consistent with emerging rules of chicken genomics, and a pictorial analysis of the "genomic signature" of this sequence, the first of its kind for birds, bears strong similarity to mammalian signatures, suggesting common higher-order structures in these homeothermic genomes. The house finch sequence is among a very few of its kind from nonmodel vertebrates and provides insight into the evolution of the avian Mhc and of avian genomes generally.[The sequence data described in this paper have been submitted to the GenBank data library under accession nos. AF205032 and AF241546-AF241565.]Long DNA sequences provide one source of the genomic information that will revolutionize biology, yet cosmid-scale (25-40 kb) or longer DNA sequences are still almost exclusively confined to model organisms and microbial pathogens. Whereas several nonmodel mammal species are the focus of large-scale mapping and genome projects (O'Brien et al. 1999), cosmidscale sequences of nonmammalian organisms are available only from chickens, Japanese quail, zebrafish, and pufferfish. We expect the genomic features gleaned from such models to predict aspects of the genomes of related species in their respective clades. Nonetheless, the full diversity of genomic structures will not be appreciated until a much larger number of genomes and DNA sequences from nonmodel species are investig...

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Base Compositional Bias and Phylogenetic Analyses: A Test of the “Flying DNA” Hypothesis

Cited by 46 publications

References 51 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

Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats

MHC Class II Pseudogene and Genomic Signature of a 32-kb Cosmid in the House Finch (Carpodacus mexicanus)

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