Variation of the Mitochondral Genome in the Evolution of Drosophila (original) (raw)

Evolution of Drosophila mitochondrial DNA and the history of the melanogaster subgroup

Proceedings of the National Academy of Sciences, 1990

The nucleotide sequences of a common region of 15 mitochondrial DNAs (mtDNAs) sampled from the Drosophila melanogaster subgroup were determined. The region is 2527 base pairs long, including most of the NADH dehydrogenase subunit 2 and cytochrome oxidase subunit 1 genes punctuated by three tRNA genes. The comparative study revealed (i) the extremely low saturation level of transitional differences, (ii) recombination or variable substitution rates even within species, (iii) long persistence times of distinct types of mtDNA in Drosophila simulans and Drosophila mauritiana, and (iv) an apparent lack of within-type variations in island species. Also found was a high correlation among the transitional rate, the saturation level, and the G+C content (or codon usage). It appears that D. simulans and D. mauritiana have maintained highly structured populations for more than 1 million years. Such structures are consistent with the origination of Drosophila sechellia from D. simulans. Yet geographic isolation is so weak as to show no evidence for further speciation. Moreover, one type of mtDNA shared by D. simulans and D. mauritiana suggests either recent divergence or ongoing introgression.

Mitochondrial DNA Evolution in the Drosophila obscura Group

1988

We report a restriction-site study of the mitochondrial DNA (mtDNA) of seven species of the Drosophila obscura group. One species (D. azteca) belongs to the afinis subgroup; the other six species are classified in the obscura subgroup, three of them being from the old-world species (D. obscura, D. ambigua, and D. subobscura) and three from the new-world species (D. pseudoobscura, D. persimilis, and D. miranda). The mtDNA patterns suggest that the phylogeny of the group needs to be revised. The Nearctic obscura species appear as more closely related to D. azteca (afinis subgroup) than to the Palearctic species. The three Palearctic species are, in turn, a very heterogeneous group, with D. obscura no more closely related to D. subobscura and D. ambigua than to D. a&is or the Nearctic obscura species. The rates of mtDNA evolution are variable: some lineages have evolved at rates two or three times greater than others. If an average rate of 0.5% nucleotide substitutions/Myr is assumed, the divergence among the four main lineages in the phylogeny would have occurred 12-l 5 Myr ago, during the Miocene, which is consistent with biogeographic information.

Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup

2000

In this study, a comparative genomics approach is employed to investigate the forces that shape evolutionary change in the mitochondrial DNA (mtDNA) of members of the Drosophila melanogaster subgroup. This approach facilitates differentiation of the patterns of variation resulting from processes acting at a higher level from those acting on a single gene. The mitochondrial genomes of three isofemale lines of D. simulans (siI, -II, and -III), two of D. melanogaster (Oregon R and a line from Zimbabwe), and D. mauritiana (maI and -II), and one of D. sechellia were sequenced and compared with that derived from D. yakuba. Data presented here indicate that at least three broad mechanisms shape the evolutionary dynamics of mtDNA in these taxa. The first set of mechanisms is intrinsic to the molecule. Dominant processes may be interpreted as selection for an increased rate of replication of the mtDNA molecule, biases in DNA repair, and differences in the pattern of nucleotide substitution among strands. In the genes encoded on the major strand (62% of the coding DNA) changes to or from C predominate, whereas on the minor changes to or from G predominate. The second set of mechanisms affects distinct lineages. There are evolutionary rate differences among lineages, possibly owing to population demographic changes or changes in mutational biases. This is supported by the heterogeneity found in synonymous, nonsynonymous, and silent substitutions. The third set of mechanisms differentially affects distinct genes. A maximum-likelihood slidingwindow analysis detected four disjunct regions that have a significantly different nucleotide substitution process from that derived from the complete sequence. These data show the potential for comparative genomics to tease apart subtle forces that shape the evolution of DNA.

Drosophila melanogaster mitochondrial DNA: gene organization and evolutionary considerations

Genetics, 1988

The sequence of a 8351-nucleotide mitochondrial DNA (mtDNA) fragment has been obtained extending the knowledge of the Drosophila melanogaster mitochondrial genome to 90% of its coding region. The sequence encodes seven polypeptides, 12 tRNAs and the 3' end of the 16S rRNA and CO III genes. The gene organization is strictly conserved with respect to the Drosophila yakuba mitochondrial genome, and different from that found in mammals and Xenopus. The high A + T content of D. melanogaster mitochondrial DNA is reflected in a reiterative codon usage, with more than 90% of the codons ending in T or A, G + C rich codons being practically absent. The average level of homology between the D. melanogaster and D. yakuba sequences is very high (roughly 94%), although insertion and deletions have been detected in protein, tRNA and large ribosomal genes. The analysis of nucleotide changes reveals a similar frequency for transitions and transversions, and reflects a strong bias against G + C o...

Divergence of Mitochondrial Dna is Not Corroborated by Nuclear Dna, Morphology, or Behavior in Drosophila Simulans

Evolution, 2002

We ask whether the observed mitochondrial DNA (mtDNA) population subdivision of Drosophila simulans is indicative of organismal structure or of specific processes acting on the mitochondrial genome. Factors either intrinsic or extrinsic to the host genome may influence the evolutionary dynamics of mtDNA. Potential intrinsic factors include adaptation of the mitochondrial genome and of nucleomitochondrial gene complexes specific to the local environment. An extrinsic force that has been shown to influence mtDNA evolution in invertebrates is the bacterial endosymbiont Wolbachia. Evidence presented in this study suggests that mtDNA is not a good indicator of organismal subdivision in D. simulans. Furthermore, there is no evidence to suggest that Wolbachia causes any reduction in nuclear gene flow in this species. The observed differentiation in mtDNA is not corroborated by data from NADH: ubiquinone reductase 75kD subunit precursor or the Alcohol dehydrogenase-related loci, from the shape or size of the male genital arch, or from assortative premating behavior. We discuss these results in relation to a mitochondrial genetic species concept and the potential for Wolbachia-induced incompatibility to be a mechanism of speciation in insects. We conclude with an iterated appeal to include phylogenetic and statistical tests of neutrality as a supplement to phylogenetic and population genetic analyses when using mtDNA as an evolutionary marker.

Evolution of Mitochondrial DNA in Drosophila subobscura

Proceedings of The National Academy of Sciences, 1986

The colonization of the New World by the Palearctic species Drosophila subobscura was first detected in 1978 in South America and around 1982 in western North America. The ensuing dramatic expansion of the species, in territory as well as numbers, provides an opportunity for studying evolution in a scale rarely possible. We have used 10 restriction endonucleases to analyze the mitochondrial DNA (mtDNA) of individuals from 23 widely dispersed localities. Only two mtDNA composite morphs have been detected in the Americas. None of the two morphs has been found in Africa, and only one in the Atlantic islands; but both are widespread in Europe, which provides no clue of the precise geographic origin of the colonizers. The amount of nucleotide-substitution polymorphism detected in D. subobscura is typical for animals, but it is greater in the Old than in the New World, presumably due to the recent colonization by a limited number of colonizers. Assuming standard evolutionary rates of mtDNA base substitution, the mtDNA morphs found in D. subobscura can be traced to a single one that existed no less than one million years ago. We argue against the inference that the D. subobscura flies now living descend from only one or a few females that lived at that time. This type of inference, which we call the "Mother Eve hypothesis," has been made to conclude that the human population went through a severe constriction about 200,000 years ago, so that all living humans descend from only one or a few women who lived at that time. The Mother Eve hypothesis is fallacious.

Mitochondrial DNA Variation and Genetic Structure in Old-World Populations of Drosophila subobscura

To discover the relation between mitochondrial DNA (mtDNA) polymorphism and the geographic population structure of Drosophila subobscura previously established for other genetic traits, a wide Paleartic survey was carried out. A total of 24 nucleomorphs was observed among 26 1 isofemale lines assayed by 11 restriction endonucleases with 38 different sites in the mtDNA cleavage map. The differentiation of the Canary Islands populations (6 = 0.0119) compared with the mean among all the other continental and insular populations (6 = 0.0002) is striking. Both the great divergence among Canary Islands nucleomorphs (6 = 0.02 1) compared with the maximum nucleomorph distance in all other populations (6 = 0.0 17) and the abundance of endemic nucleomorphs (11) on the Canary Islands (50% of the total number of different nucleomorphs found in the entire distribution area) suggest that this molecular differentiation most probably results from the very old age of the Canary Islands populations rather than from drift and founder effects.

The rate and pattern of nucleotide substitution in Drosophila mitochondrial DNA

Molecular Biology and Evolution, 1992

The nucleotide sequences of a segment of mitochondrial DNA (mtDNA) have been determined for nine species or subspecies of the subgenus Drosophila of the genus Drosophila. This segment contains two complete protein-coding genes (i.e., NADH dehydrogenase subunit 1 and cytochrome b) and a transfer RNA gene (tRNA ,'). The G+C content at third-codon positions for the two protein-coding genes was 1.5 times higher than that in the D. melanogaster species group, which belongs to the subgenus Sophophora. However, there was a substantial difference between the nucleotide frequencies of G and C. The number of nucleotide substitutions per silent site was more than three times higher than that for nuclear DNA, although it was only 60% of that for mammalian mtDNA. Both parametric and nonparametric analyses revealed a strong transition-transversion bias in nucleotide substitution, as was observed in mammalian mtDNA. Moreover, the rate of substitution of A and T for G and C is higher than that for the opposite direction. This bias seems to be responsible for the extremely A+T-rich base composition of Drosophila mtDNA. It is also noted that the rate of transitional change between A and G is higher than that between T and C.

Analysis of nucleotide substitutions of mitochondrial DNAs in Drosophila melanogaster and its sibling species

Molecular Biology and Evolution

To study the rate and pattern of nucleotide substitution in mitochondrial DNA (mtDNA), we cloned and sequenced a 975-bp segment of mtDNA from Drosophila melanogaster, D. simulans, and D. mauritiana containing the genes for three transfer RNAs and parts of two protein-coding genes, ND2 and COI. Statistical analysis of synonymous substitutions revealed a predominance of transitions over transversions among the three species, a finding differing from previous results obtained from a comparison of D. melanogaster and D. yakuba. The number of transitions observed was nearly the same for each species comparison, including D. yakuba, despite the differences in divergence times. However, transversions seemed to increase steadily with increasing divergence time. By contrast, nonsynonymous substitutions in the ND2 gene showed a predominance of transversions over transitions. Most transversions were between A and T and seemed to be due to some kind of mutational bias to which the A+T-rich mtDNA of Drosophila species may be subject. The overall rate of nucleotide substitution in Drosophila mtDNA appears to be slightly faster (-1.4 times) than that of the Adh gene. This contrasts with the result obtained for mammals, in which the mtDNA evolves-10 times faster than single-copy nuclear DNA. We have also shown that the start codon of the CO1 gene is GTGA in D. simulans and GTAA in D. mauritiana. These codons are different from that of D. melanogaster (ATAA).

Mitochondrial genome size variation in New World and Old World populations of Drosophila melanogaster

Heredity, 2004

Drosophila melanogaster originated in Africa, spread to Europe and Asia, and is believed to have colonized the New World in the past few hundred years. Levels of genetic variation are typically reduced in New World populations, consistent with a founder event following range expansion out of Africa and the Old World. We describe the patterns of mtDNA length variation within and among several populations of Drosophila melanogaster from the Old and New World. MtDNA length variation is due to insertion and deletion of tandem repeats in the control region (D-loop) of D. melanogaster mitochondrial genome. The distinct mutational dynamics of this system provide an opportunity to compare the patterns of variation in this marker to those of other markers with different mutational pressures and linkage relationships. The data show significantly more length variation in African and Asian samples than in New World samples. New World samples also show more pronounced skew of the length distribution. Our results are distinct from an earlier study that showed significantly higher levels of length variation and heteroplasmy. The level of heteroplasmy is highly correlated with the number of years that samples have been maintained in laboratory culture, suggesting that relaxed selection in small populations permits the accumulation of mtDNA length variation and heteroplasmy. Together, the data indicate that mtDNA length variants retain a signature of founder events and selection, and suggest that further investigation into the mutation-selection dynamics of the D-loop region of mtDNA would provide a distinct and informative marker for analysis of the recent history of populations.