Skip Navigation


MBE Advance Access originally published online on June 27, 2003
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Material
Right arrow All Versions of this Article:
20/10/1612    most recent
msg176v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (26)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Shao, R.
Right arrow Articles by Barker, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shao, R.
Right arrow Articles by Barker, S. C.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

Mol. Biol. Evol. 20(10):1612-1619. 2003
DOI: 10.1093/molbev/msg176
© 2003 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

Rates of Gene Rearrangement and Nucleotide Substitution Are Correlated in the Mitochondrial Genomes of Insects

Renfu Shao*,, Mark Dowton{dagger}, Anna Murrell* and Stephen C. Barker*

* Department of Microbiology and Parasitology, and Institute for Molecular Bioscience, The University of Queensland, Brisbane, Australia
{dagger} Institute of Conservation Biology, Department of Biology, Wollongong University, Wollongong, Australia

E-mail: r.shao{at}mailbox.uq.edu.au.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 Acknowledgements
 Literature Cited
 
A number of studies indicated that lineages of animals with high rates of mitochondrial (mt) gene rearrangement might have high rates of mt nucleotide substitution. We chose the hemipteroid assemblage and the Insecta to test the idea that rates of mt gene rearrangement and mt nucleotide substitution are correlated. For this purpose, we sequenced the mt genome of a lepidopsocid from the Psocoptera, the only order of hemipteroid insects for which an entire mtDNA sequence is not available. The mt genome of this lepidopsocid is circular, 16,924 bp long, and contains 37 genes and a putative control region; seven tRNA genes and a protein-coding gene in this genome have changed positions relative to the ancestral arrangement of mt genes of insects. We then compared the relative rates of nucleotide substitution among species from each of the four orders of hemipteroid insects and among the 20 insects whose mt genomes have been sequenced entirely. All comparisons among the hemipteroid insects showed that species with higher rates of gene rearrangement also had significantly higher rates of nucleotide substitution statistically than did species with lower rates of gene rearrangement. In comparisons among the 20 insects, where the mt genomes of the two species differed by more than five breakpoints, the more rearranged species always had a significantly higher rate of nucleotide substitution than the less rearranged species. However, in comparisons where the mt genomes of two species differed by five or less breakpoints, the more rearranged species did not always have a significantly higher rate of nucleotide substitution than the less rearranged species. We tested the statistical significance of the correlation between the rates of mt gene rearrangement and mt nucleotide substitution with nine pairs of insects that were phylogenetically independent from one another. We found that the correlation was positive and statistically significant (R2 = 0.73, P = 0.01; Rs = 0.67, P < 0.05). We propose that increased rates of nucleotide substitution may lead to increased rates of gene rearrangement in the mt genomes of insects.

Key Words: hemipteroid • Psocoptera • mitochondrial clock • molecular evolution • rate heterogeneity


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 Acknowledgements
 Literature Cited
 
The rate of nucleotide substitution in animal mitochondrial (mt) genomes varies substantially among lineages (Crozier, Crozier, and Mackinlay 1989; Martin and Palumbi 1993; Dowton and Austin 1995; Hoeh et al. 1996; Page et al. 1998; Gissi et al. 2000; Krieger and Fuerst 2002). The rate of mt gene rearrangement also varies substantially among lineages, especially among lineages of invertebrates (Hoffmann, Boore, and Brown 1992; Boore and Brown 1994; Black and Roehrdanz 1998; Campbell and Barker 1998, 1999; Boore 1999; Dowton and Austin 1999; Yokobori et al. 1999; Shao, Campbell, and Barker 2001; Shao et al. 2001; Shao and Barker 2003). Although nucleotide substitution and gene rearrangement are two distinct mutational phenomena, a number of studies have indicated that they might be correlated in animal mt genomes, since a number of lineages have both a high rate of mt gene rearrangement and a high rate of nucleotide substitution; for example, the lineages of the blue mussel, Mytilus edulis (Hoffmann, Boore, and Brown 1992; Hoeh et al. 1996), the akamata snake, Dinodon semicarinatus (Kumazawa et al. 1998), the ascidian, Halocynthia roretzi (Yokobori et al. 1999), some hymenopterans (Crozier, Crozier, and Mackinlay 1989; Crozier and Crozier 1993; Dowton and Austin 1995, 1999), and some lice (Page et al. 1998; Shao, Campbell, and Barker 2001). However, no one has tested systematically the idea that the rate of mt gene rearrangement and the rate of mt nucleotide substitution are correlated. Doubtless, this is due to the lack of suitable model systems. An ideal model system would have lineages with a range of rates of mt gene rearrangement. The hemipteroid assemblage (see below and Shao and Barker [2003]) and the Insecta (see below) seem to meet this requirement.

The hemipteroid assemblage has four orders of insects: Hemiptera (bugs, cicadas, whiteflies, aphids, etc.), Phthiraptera (lice), Psocoptera (psocids, book lice, and bark lice), and Thysanoptera (thrips). The rate of mt gene rearrangement varies substantially in the hemipteroid assemblage. Compared with the inferred ancestral arrangement of mt genes of insects (Shao, Campbell, and Barker 2001), no rearrangements have been found in the Hemip-tera (Shao et al. 2001). In contrast, 24 genes have rearranged in the plague thrips, Thrips imaginis (Thysanoptera [Shao and Barker 2003]), and 31 genes have rearranged in the wallaby louse, Heterodoxus macropus (Phthiraptera [Shao, Campbell, and Barker 2001]). The nucleotide sequence of a 1.8-kb fragment of the mt genome of a lepidopsocid (Psocoptera) indicated a level of rearrangement in this species intermediate to that of the Hemiptera and the plague thrips (Shao et al. 2001). In the present study, we sequenced the entire mt genome of this lepidopsocid and found that eight genes have rearranged in this genome.

Other lineages of insects also vary in the rate of mt gene rearrangement. The three species of Coleoptera sequenced entirely have the ancestral gene arrangement of insects (see table 1). Five of the seven species of Diptera sequenced entirely also have the ancestral arrangement, whereas two species of Diptera, Anopheles quadrimaculatus and A. gambiae, have two tRNA genes rearranged. Four species of Lepidoptera and the locust, Locusta migratoria (Orthoptera), have a single tRNA gene rearranged, and the honeybee, Apis mellifera (Hymenoptera), has eight tRNA genes rearranged. Thus, the Insecta has lineages with low rates, intermediate rates, and high rates of mt gene rearrangement.


View this table:
[in this window]
[in a new window]
  		Table 1 Species of Insects and a Crustacea Studied.

 
We compared the relative rates of mt nucleotide substitution among the four orders of hemipteroid insects and among all of the insects whose mt genomes have been sequenced entirely. We then tested the degree of correlation between the rate of gene rearrangement and the rate of nucleotide substitution among nine pairs of insects that are phylogenetically independent from one another. We found that there was a statistically significant correlation between the rate of gene rearrangement and the rate of nucleotide substitution in the mt genomes of these insects. We propose that increased rates of nucleotide substitution may lead to increased rates of gene rearrangement in the mt genomes of insects.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 Acknowledgements
 Literature Cited
 
Sequencing of the Mitochondrial Genome of the Lepidopsocid
The lepidopsocid was an undescribed species in the family Lepidopsocidae; the specimen was collected by Dr. Evan Schmidt in the Brisbane Forest Park, Queensland, Australia. A voucher specimen was deposited in the Queensland Museum (Register Number QMT93416). DNA extraction and the nucleotide sequence of a 1.8-kb fragment of the mt genome of the lepdopsocid was reported in Shao et al. (2001). In the present study, we amplified the entire mt genome of the lepidopsocid in seven overlapping fragments (fig. 1) with the following primers: (1) C1-J-1718 and C3-N-5460 (3,083-bp fragment); (2) C1-J-2177 and C2-N-3661 (3,741-bp fragment), (3) C2-J-3400 and N5-N-7736 (2,368-bp fragment); (4) N5-J-7567 and N1-N-12595 (4,983-bp fragment); (5) N4-J-8944 and LR-N-12866 (3,849-bp fragment); (6) N1-J-12636 (5'-GCTACTCCTACAAGAATTCC-3') and LR-N-13609 (5'-AGTTTAATTTAAAATTGTAC-3'; 1,002-bp fragment); and (7) LR-J-12889 (5'-ACGCCGGTCTGAACTCAAATCATGTAA-3') and C1-N-2161 (6,151-bp fragment; only the sequences of primers reported here for the first time are shown; see Simon et al. [1994], Shao, Campbell, and Barker [2001], and Shao et al. [2001] for the sequences of the other primers). Elongase Enzyme Mix (GIBCO BRL®) was used in PCR. The cycling conditions were 1 min at 94°C followed by 35 to 40 cycles of 30 sec at 40°C to 50°C (depending on primers), 1 to 7 min (~1 min/kb) at 68°C or 60°C, and then 2 to 10 min at 68°C or 60°C. The extension temperature was 68°C for the first six fragments. The seventh fragment, which includes the entire control region of the mt genome, failed to be amplified at 68°C but was amplified successfully at 60°C. The PCR fragments were purified with QIAquick PCR Purification Kit (Qiagen) and sequenced directly with internal primers, except for a 2,838-bp region in the seventh fragment. This region comprises part of rrnS, the entire control region, trnQ, and part of nad2. Direct sequencing reactions repeatedly failed from both sides of this region. So, we cloned the PCR products amplified from this region with pGEM®-T Easy Vector System and sequenced this region with M13 primers and internal primers. The nucleotide sequences of both strands were determined for the entire mt genome (GenBank accession number AF335994).



View larger version (28K):
[in this window]
[in a new window]
  		FIG. 1. Comparison of the arrangement of genes in the mitochondrial genome of the lepidopsocid (Psocoptera) with that of the hypothetical ancestral insect. These circular genomes have been linearized at the 5' end of cox1. Lines at the top show the seven overlapping PCR fragments from which the mitochondrial genome of the lepidopsocid was sequenced. Genes are transcribed from left to right except those whose names are underlined, which are transcribed from right to left. The protein-coding genes and rRNA genes are atp6 and atp8 (encoding ATP synthase subunits 6 and 8), cox1 to cox3 (cytochrome oxidase subunits 1 to 3), cob (cytochrome b), nad1 to nad6 and nad4L (NADH dehydrogenase subunits 1 to 6 and 4L), and rrnL and rrnS (large and small ribosomal RNA subunits). The tRNA genes are labeled with their single-letter amino acid abbreviations except for those that encode leucine and serine, which are labeled L1 (anticodon tag), L2 (TAA), S1 (GCT), and S2 (TGA). CR is the abbreviation for the putative control region. Lines with arrows indicate translocations of genes from their hypothetical ancestral positions to their positions in the lepidopsocid. Genes that may have translocated as a block are marked with a thick horizontal line

 
Relative Rate Tests of Nucleotide Substitution
The amino acid sequences of the 13 mt protein-coding genes of the lepidopsocid, 19 other insects, and the crustacean Daphnia pulex (table 1) were aligned with ClustalW version 1.8 (Thompson, Higgins, and Gibson 1994). CodonAlign 1.0 (http://www.rochester.edu/College/BIO/labs/HallLab/CodonAlign.html) was then used to align the nucleotide sequences of these protein-coding genes with reference to the alignment of amino acid sequences. The 13 nucleotide sequence alignments were then concatenated into one data set (see Supplementary Material online). Relative-rate tests were executed with RRTree version 1.1 (Robinson-Rechavi and Huchon 2000).

There are six pairwise comparisons among the four hemipteroid insects and 45 pairwise comparisons among the 20 insects (table 2)—species of insects that have identical gene arrangements and are in the same taxonomic order were treated as a single lineage in the relative-rate tests. These species are (1) the five dipterans that have the ancestral gene arrangement of insects, (2) the two dipterans (Anopheles spp.) that have two genes rearranged, (3) the four lepidopterans that have one gene rearranged, and (4) the three coleopterans that have the ancestral gene arrangement of insects. We compared Ks (number of synonymous substitutions per synonymous site), Ka (number of nonsynonymous substitutions per nonsynonymous site), and B4 (number of synomymous transversions per fourfold degenerate site).


View this table:
[in this window]
[in a new window]
  		Table 2 Comparisons of the Relative Rates of Gene Rearrangement and Nucleotide Substitution Among Hemipteroid Insects and Among All of the 20 Insects Whose Mitochondrial Genomes Have been Sequenced Entirely.

 
Relative Rate Tests of Mitochondrial Gene Rearrangement
To assess the relative numbers of gene rearrangements between mt genomes of two taxa, we used the breakpoint (BP) distance (as described in Blanchette, Kunisawa, and Sankoff. [1999]). This calculates the minimum number of BPs that must be introduced into one genome to change it to the other genome. In the simplest comparison, two genomes that differ by the placement of a single gene have a BP of 3; two BPs are needed to excise the rearranged gene from its original location, with a third BP needed to introduce that gene into its new location. The BP between pairs of taxa were calculated with Grappa version 1.6 (Moret et al. 2001).

Tests that assess the relative rate of gene rearrangement between two taxa have not been developed. So we devised such a test, using the relative-rate test of nucleotide substitution as a framework (Li and Bousquet 1992). We assessed the relative rate of gene rearrangement between pairs of taxa by reference to a third taxon (an outgroup). We calculated the BP between the outgroup and each of the ingroup taxa. The relative rate of gene rearrangement (RRTGR) was then calculated as the difference between these two BP values, or


where BP(1,3) is the breakpoint distance between taxon 1 and the outgroup (taxon 3), and BP(2,3) is the breakpoint distance between taxon 2 and the outgroup (taxon 3). In this way, the relative rate of gene rearrangement between a pair of taxa could be compared directly with the relative rate of nucleotide substitution between the same pair of taxa.

Test for Significance of the Correlation Between Rates of Gene Rearrangement and Nucleotide Substitution
We tested the correlation between the rate of gene rearrangement and the rate of nucleotide substitution for statistical significance using parametric (Pearson) and nonparametric (Spearman Rank) tests. We only used the pairs of species that were independent from one another on the phylogenetic tree (table 3 and fig. 2); this is because the inclusion of nonindependent pairs of species may overestimate the degree of correlation by using the same data more than once (Felsenstein 1985). Among the 20 insects whose mt genomes have been sequenced entirely, there were nine pairs of insects that were suitable for this test. We sampled each branch in the phylogeny of these insects only once and purposefully sampled all branches along which rearrangements have occurred (fig. 2, dashed branches). Tribolium castaneum (Coleoptera) was used as an outgroup in four of the nine comparisons because it has the ancestral mt gene arrangement of insects and has a lower rate of nucleotide substitution compared with the other two species of Coleoptera sequenced entirely (data not shown). These properties made it an ideal outgroup since relative rate tests are most accurate when the mean distance of each taxon to the outgroup is smallest (Robinson et al. 1998).



View larger version (37K):
[in this window]
[in a new window]
  		FIG. 2. Phylogeny used in the test of the correlation between the rate of mitochondrial gene rearrangement and the rate of mitochondrial nucleotide substitution. This tree shows the current understanding of the interordinal phylogeny of insects (Wheeler et al. 2001). Dashed branches indicate lineages with mitochondrial gene rearrangements. Both spotted and dashed branches were sampled in our test for a correlation between the rate of mitochondrial gene rearrangement and the rate of mitochondrial nucleotide substitution. Black branches were not sampled

 

   Results and Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
Acknowledgements
 Literature Cited
 
Mitochondrial Genome of the Lepidopsocid
The mt genome of the lepidopsocid is circular and has 16,924 bp. This genome has 13 protein-coding genes, two rRNA genes, 22 tRNA genes, and a putative control region (fig. 1). The majority strand has 6,961 adenines (41%), 6,413 thymines (38%), 2,111 cytosines (12%), and 1,439 guanines (9%). The gene content and nucleotide composition of this genome are typical of the mt genomes of insects (Clary and Wolstenholme 1985; Crease 1999). However, the arrangement of genes in the mt genome of this lepidopsocid is not typical for an insect since seven tRNA genes (R, S1, E, S2, I, M, and W) and a protein-coding gene (cox2) have changed positions relative to the ancestral arrangement of insects (fig. 1). The number of mt genes that have rearranged in this lepidopsocid (eight genes rearranged; Psocoptera) is less than that in Heterodoxus macropus (31 genes rearranged; Phthiraptera) and Thrips imaginis (24 genes rearranged; Thysanoptera), the same as that in Apis mellifera (eight genes rearranged; Hymenoptera), but greater than that in all other insects studied (table 1).

Relative Rates of Nucleotide Substitution and Gene Rearrangement
RRTree tests indicated that Ks (number of synonymous substitutions per synonymous site) was saturated in 53 of the 60 pairwise comparisons in tables 2 and 3. In the other seven comparisons in which Ks was not saturated, there was no significant variation in Ks between the two taxa compared. Saturation plots of corrected and uncorrected pairwise distances of first, second, and third codon positions also indicated extreme saturation at the third codon position, where corrected distances were frequently greater than 1.0 (data not shown). There was no significant variation in B4 (number of synonymous transversions per fourfold degenerate site) in any of the 60 pairwise comparisons. However, there was significant variation in Ka (number of nonsynonymous substitutions per nonsynonymous site) in 49 of the 60 comparisons. Together, these observations indicate that neither Ks nor B4 is a good proxy or measure for nucleotide substitution rate when examining highly divergent organisms (e.g., in our case, species across nine taxonomic orders of insects). Therefore, only the rates of non-synonymous substitutions were shown in tables 2 and 3.


View this table:
[in this window]
[in a new window]
  		Table 3 Nine Phylogenetically Independent Pairs of Insects Used in the Test of the Correlation Between the Rates of Gene Rearrangement and Nucleotide Substitution.

 
All six comparisons among the four hemipteroid insects show that species with high rates of gene rearrangement also have high rates of nucleotide substitution (table 2). The hierarchy of the rate of nucleotide substitution was Heterodoxus macropus > Thrips imaginis > lepidopsocid > Triatoma dimidiata. This hierarchy did not change whether Drosophila yakuba (Diptera), Tribolium castaneum (Coleoptera), Bombyx mori (Lepidoptera), or Locusta migratoria (Orthoptera) was the outgroup. The hierarchy of the rate of nucleotide substitution was the same as the hierarchy of the rate of mt gene rearrangement of these hemipteroid insects: Heterodoxus macropus (35 breakpoints) > Thrips imaginis (30 breakpoints) > lepidopsocid (15 breakpoints) > Triatoma dimidiata (0 breakpoints).

To test whether the correlation between the rate of gene rearrangement and the rate of nucleotide substitution in these hemipteroid insects is a more general phenomenon, we tested the relative rates of mt gene rearrangement and mt nucleotide substitution among all 20 species of insects whose mt genomes have been sequenced entirely. The crustacean Daphnia pulex was the outgroup (table 2). The hierarchy of rate of nucleotide substitution of these 20 insects was Heterodoxus macropus {approx}Thrips imaginis > Apis mellifera > lepidopsocid > Triatoma dimidiata > Locusta migratoria {approx}Lepidoptera {approx}Coleoptera {approx}Diptera (Anopheles spp. excluded) > Anopheles spp. ("{approx}" indicates no significant difference). This hierarchy is similar but not identical to the hierarchy of the rate of mt gene rearrangement of these insects: Heterodoxus macropus (35 breakpoints) > Thrips imaginis (30 breakpoints) > Apis mellifera (16 breakpoints) > lepidopsocid (15 breakpoints) > Locusta migratoria (3 breakpoints) = Lepidoptera (3 breakpoints) > Anopheles spp. (1 breakpoint) > Triatoma dimidiata (0 breakpoints) = Coleoptera (0 breakpoints) = Diptera (0 breakpoints). The major difference between the two hierarchies is due to the positions of the Anopheles spp. and Triatoma dimidiata (underlined in the hierarchy of the rate of mt gene rearrangement above). In 28 of the 45 comparisons where the two lineages differed by more than five breakpoints, the more rearranged lineage always had a statistically significantly higher rate of nucleotide substitution than the less rearranged lineage. The average difference for these 28 comparisons was 0.1680. In the 17 other comparisons where the two lineages differed by five or less breakpoints, the more rearranged lineage did not always have a higher rate of nucleotide substitution than the less rearranged lineage. The average difference for these 17 comparisons was 0.0280. In some cases, the less rearranged lineage had a significantly higher rate of nucleotide substitution than the more rearranged lineage (the comparisons with negative values of BP(1,3) – BP(2,3) in table 2).

Correlation Between Rate of Gene Rearrangement and Rate of Nucleotide Substitution
Table 2 shows that the lineages with high rates of gene rearrangement generally have high rates of nucleotide substitution. However, table 2 does not show if the correlation between the rate of gene rearrangement and the rate of nucleotide substitution is statistically significant or not. We tested the statistical significance of the correlation between the rate of gene rearrangement and the rate of nucleotide substitution by comparing these rates in nine phylogenetically independent pairs of species (table 3).The rate of gene rearrangement and the rate of nucleotide substitution were positively correlated and the degree of correlation was statistically significant: Pearson R2= 0.73, P = 0.01 and Spearman Rank Rs = 0.67, P < 0.05 (fig. 3).



View larger version (10K):
[in this window]
[in a new window]
  		FIG. 3. Correlation between the rate of mitochondrial gene rearrangement and the rate of nucleotide substitution among insects. Differences in the minimum number of breakpoints between two lineages BP(1,3) – BP(2,3) are along the horizontal axis, whereas differences in the number of nonsynonymous substitutions per nonsynonymous site (K13 – K23) between two lineages are along the vertical axis

 
Possible Role of Nucleotide Substitution in the Rearrangement of Mitochondrial Genes of Insects
A number of factors seem to affect the rate of nucleotide substitution in vertebrates, including (1) efficiency of DNA repair—the less efficient the repair mechanism, the higher the substitution rate (Britten 1986); (2) metabolic rate—the higher the metabolic rate, the higher the substitution rate (Martin, Naylor, and Palumbi 1992; Martin and Palumbi 1993); (3) generation time—the shorter the generation time, the higher the substitution rate (Li et al. 1996); and (4) body size—the smaller the body size, the higher the substitution rate (Martin and Palumbi 1993; Bromham 2002). Studies on insects also indicated that population size (Ohta 1993; Crozier, Crozier, and Mackinlay 1989) and parasitic lifestyle (Dowton and Austin 1995) may be linked to the rate of nucleotide substitution.

Little is known about the factors that affect the rate of gene rearrangement in mt genomes of animals. The rate of mt gene rearrangement was thought to be universally low in animals since the arrangement of mt genes is identical in most lineages of vertebrates (Boore 1999). However, a low rate of mt gene rearrangement seems to be peculiar to vertebrates. The rate of mt gene rearrangement varies substantially in the Insecta (see above) and in other lineages of arthropods; for example, the Crustacea (Tigriopus japonicus [Machida et al. 2002]), the ticks (Chelicerata [Black and Roehrdanz 1998; Campbell and Barker 1998, 1999]) and the millipedes (Myriapoda [Lavrov, Boore, and Brown 2002]). Indeed, most groups of invertebrates have lineages with many rearrangements and lineages with few rearrangements; for example, Mollusca, Nematoda, Platyhelminthes, Cnidaria, Echinodermata, and Brachiopoda (Boore 1999).

So, why is the rate of mt gene rearrangement high in some lineages of animals but low in others? We propose that the statistically significant correlation between the rate of mt nucleotide substitution and the rate of mt gene rearrangement in insects may point to an answer to this question. Our hypothesis is that a high rate of nucleotide substitution may lead to a high rate of mt gene rearrangement. There are three steps in our hypothesis. First, one or more of the four biochemical and life history traits listed above evolves in a lineage; that is, there may be a decrease in efficiency of DNA repair, increase in metabolic rate, decrease in generation time, and/or decrease in body size. Second, these changes cause the rate of nucleotide substitution to increase in mt genomes. Third, a high rate of nucleotide substitution leads to an increase in mutation at the sites of initiation and termination of the mt genome replication and causes errors during replication of mt genomes. These errors then cause gene rearrangements through duplication and deletion mechanism (Boore 2000; Lavrov, Boore, and Brown 2002) and lead to an increase in the rate of mt gene rearrangement. It is possible that other mechanisms, in addition to the duplication and deletion mechanism, may also cause a high rate of gene rearrangement from a high rate of nucleotide substitution. For example, a high rate of endogenous DNA damage, due to a high rate of nucleotide substitution, may result in a high rate of double-strand breaks that may cause illegitimate recombination (Boore 2000) or intramitochondrial recombination (Dowton and Campbell 2001). Alternatively, the organisms with high substitution rates may have relaxed selection; thus mtDNA rearrangement are tolerated more than in species with low substitution rates.

Of course, other as yet undiscovered factors may also affect the rate of gene rearrangement in the mt genomes of animals. For example, we speculate that life histories and ecologies that tend to cause genetic founder effects, such as the life history of lice, psocopterans, and thrips, may increase the chance that rearranged mt genomes survive and become fixed in populations. Further studies on hemipteroid insects on such factors should be instructive.


   Acknowledgements
TOP
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 Acknowledgements
Literature Cited
 
We thank Evan Schmidt for collecting and identifying the lepidopsocid specimen, and Min Hu for suggestion on cycling condition (see Hu, Chilton, and Gasser 2002). We also thank the anonymous reviewers and the review editor for comments and suggestions that greatly improved our manuscript. R.S. was a Ph.D. student sponsored by an International Postgraduate Research Scholarship and a University of Queensland International Postgraduate Research Scholarship. S.C.B. is a member of the ARC Special Research Centre for Functional and Applied Genomics.


   Footnotes
 
Richard Thomas, Associate Editor Back


   Literature Cited
TOP
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 Acknowledgements
 Literature Cited
 

    Beard, C. B., D. M. Hamm, and F. H. Collins. 1993. The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol. Biol. 2:103-104.[Medline]

    Black, W. C., and R. L. Roehrdanz. 1998. Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Mol. Biol. Evol. 15:1772-1785.[Abstract]

    Blanchette, M., T. Kunisawa, and D. Sankoff. 1999. Gene order breakpoint evidence in animal mitochondrial phylogeny. J. Mol. Evol. 49:193-203.[CrossRef][ISI][Medline]

    Boore, J. L. 1999. Animal mitochondrial genomes. Nucleic Acid Res. 27:1767-1780.[Abstract/Free Full Text]

    Blanchette, M, T. Kunisawa, and D. Sankoff. 2000. The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. Pp. 133–147 in D. Sankoff and J. H. Nadeau, eds. Comparative genomics. Kluwer Academic Publishers, The Netherlands.

    Boore, J. L., and W. M. Brown. 1994. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138:423-443.[Abstract]

    Britten, R. J. 1986. Rates of DNA sequence evolution differ between taxonomic groups. Science 231:1393-1398.[Abstract/Free Full Text]

    Bromham, L. 2002. Molecular clocks in reptiles: life history influences rate of molecular evolution. Mol. Biol. Evol. 19:302-309.[Abstract/Free Full Text]

    Campbell, N. J. H., and S. C. Barker. 1998. An unprecedented major rearrangement in an arthropod mitochondrial genome. Mol. Biol. Evol. 15:1786-1787.[ISI][Medline]

    Campbell, N. J. H., and S. C. Barker. 1999. The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplus: fivefold tandem repetition of a coding region. Mol. Biol. Evol. 16:732-740.[Abstract]

    Clary, D. O., and D. R. Wolstenholme. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. 22:252-271.[CrossRef][ISI][Medline]

    Crease, T. J. 1999. The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:89-99.[CrossRef][ISI][Medline]

    Crozier, R. H., and Y. C. Crozier. 1993. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133:97-117.[Abstract]

    Crozier, R. H., Y. C. Crozier, and A. G. Mackinlay. 1989. The CO-I and CO-II region of honeybee mitochondrial DNA: evidence for variation in insect mitochondrial evolutionary rates. Mol. Biol. Evol. 4:399-411.

    Dotson, E. M., and C. B. Beard. 2001. Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Mol. Biol. 10:205-215.[CrossRef][ISI][Medline]

    Dowton, M., and A. D. Austin. 1995. Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. J. Mol. Evol. 41:958-965.[ISI][Medline]

    Dowton, M., and A. D. Austin. 1999. Evolutionary dynamics of a mitochondrial rearrangement "hotspot" in the Hymenoptera. Mol. Biol. Evol. 16:298-309.[Abstract]

    Dowton, M., and N. J. H. Campbell. 2001. Intramitochondrial recombination—is it why some mitochondrial genes sleep around? Trends Ecol. Evol. 16:269-271.[CrossRef][Medline]

    Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.

    Flook, P. K., C. H. F. Rowell, and G. Gellissen. 1995. The sequence, organization and evolution of the Locusta migratoria mitochondrial genome. J. Mol. Evol. 41:928-941.[ISI][Medline]

    Gissi, C., A. Reyes, G. Pesole, and C. Saccone. 2000. Lineage-specific evolutionary rate in mammalian mtDNA. Mol. Biol. Evol. 17:1022-1031.[Abstract/Free Full Text]

    Hoeh, W. R., D. T. Stewart, B. W. Sutherland, and E. Zouros. 1996. Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia). Mol. Biol. Evol. 13:418-421.[ISI][Medline]

    Hoffmann, R. J., J. L. Boore, and W. M. Brown. 1992. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131:397-412.[Abstract]

    Hu, M., N. B. Chilton, and R. B. Gasser. 2002. Long PCR-based amplification of the entire mitochondrial genome from single parasitic nematodes. Mol. Cell. Probes 16:261-267.[CrossRef][ISI][Medline]

    Krieger, J., and P. A. Fuerst. 2002. Evidence for a slowed rate of molecular evolution in the order Acipenseriformes. Mol. Biol. Evol. 19:891-897.[Abstract/Free Full Text]

    Kumazawa, Y., H. Ota, M. Nishida, and T. Ozawa. 1998. The complete nucleotide sequence of a snake (Dinodon semicarinatus) mitochondrial genome with two identical control regions. Genetics 150:313-329.[Abstract/Free Full Text]

    Lavrov, D. V., J. L. Boore, and W. M. Brown. 2002. Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Mol. Biol. Evol. 19:163-169.[Abstract/Free Full Text]

    Lessinger, A. C., A. C. M. Junqueira, T. A. Lemos, E. L. Kemper, F. R. da Silva, A. L. Vettore, P. Arruda, and A. M. L. Azeredo-Espin. 2000. The mitochondrial genome of the primary screwworm fly Cochliomyia hominivorax (Diptera : Calliphoridae). Insect Mol. Biol. 9:521-529.[CrossRef][ISI][Medline]

    Lewis, D. L., C. L. Farr, and L. S. Kaguni. 1995. Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons. Insect Mol. Biol. 4:263-278.[ISI][Medline]

    Li, P., and J. Bousquet. 1992. Relative-rate test for nucleotide substitutions between two lineages. Mol. Biol. Evol. 9:1185-1189.[ISI]

    Li, W. H., D. L. Ellsworth, J. Krushkal, B. H. Chang, and D. Hewett-Emmett. 1996. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis. Mol. Phylogenet. Evol. 5:182-187.[CrossRef][ISI][Medline]

    Machida, R. J., M. U. Miya, M. Nishida, and S. Nishida. 2002. Complete mitochondrial DNA sequence of Tigriopus japonicus (Crustacea: Copepoda). Mar. Biotech. 4:406-417.

    Martin, A. P., G. J. Naylor, and S. R. Palumbi. 1992. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153-155.[CrossRef][Medline]

    Martin, A. P., and S. R. Palumbi. 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl. Acad. Sci. USA 9:4087-4091.

    Mitchell, S. E., A. F. Cockburn, and J. A. Seawright. 1993. The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome 36:1058-1073.[Medline]

    Moret, B. M. E., S. Wyman, D. A. Bader, T. Warnow, and M. Yan. 2001. Phylogenies from gene order data: a detailed study of break-point analysis. Pp. 583–594 in R. B. Altman, A. K. Dunker, L. Hunker, K. Lauderdale, and T. E. Klein, eds. Proceedings of the 6th Pacific Symposium on Biocomputing, Hawaii. World Scientific Publication.

    Ohta, T. 1993. Amino-acid substitution at the Adh locus of Drosophila is facilitated by small population-size. Proc. Natl. Acad. Sci. USA 90:4548-4551.[Abstract/Free Full Text]

    Page, R. D., P. L. Lee, S. A. Becher, R. Griffiths, and D. H. Clayton. 1998. A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Mol. Phylogenet. Evol. 9:276-293.[CrossRef][ISI][Medline]

    Robinson, M., M. Gouy, C. Gautier, and D. Mouchiroud. 1998. Sensitivity of the relative-rate test to taxonomic sampling. Mol. Biol. Evol. 15:1091-1098.[Abstract]

    Robinson-Rechavi, M., and D. Huchon. 2000. RRTree: relative-rate tests between groups of sequences on a phylogenetic tree. Version 1.1. Bioinformatics 16:296-297.[Abstract/Free Full Text]

    Shao, R., and S. C. Barker. 2003. The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA genes. Mol. Biol. Evol. 20:362-370.[Abstract/Free Full Text]

    Shao, R., N. J. H. Campbell, and S. C. Barker. 2001. Numerous gene rearrangements in the mitochondrial genome of the wallaby louse, Heterodoxus macropus (Phthiraptera). Mol. Biol. Evol. 18:858-865.[Abstract/Free Full Text]

    Shao, R., N. J. H. Campbell, E. R. Schmidt, and S. C. Barker. 2001. Increased rate of gene rearrangement in the mitochondrial genomes of three orders of hemipteroid insects. Mol. Biol. Evol. 18:1828-1832.[Free Full Text]

    Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu, and P. Flook. 1994. Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87:651-701.

    Spanos, L., G. Koutroumbas, M. Kotsyfakis, and C. Louis. 2000. The mitochondrial genome of the Mediterranean fruit fly, Ceratitis capitata. Insect Mol. Biol. 9:139-144.[CrossRef][ISI][Medline]

    Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.[Abstract/Free Full Text]

    Wheeler, W. C., M. Whiting, Q. D. Wheeler, and J. M. Carpenter. 2001. The phylogeny of the extant hexapod orders. Cladistics 17:113-169.[CrossRef]

    Yokobori, S., T. Ueda, G. Feldmaier-Fuchs, S. Paabo, R. Ueshima, A. Kondow, K. Nishikawa, and K. Watanabe. 1999. Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata). Genetics 153:1851-1862.[Abstract/Free Full Text]

    Yukuhiro, K., H. Sezutsu, M. Itoh, K. Shimizu, and Y. Banno. 2002. Significant levels of sequence divergence and gene rearrangements have occurred between the mitochondrial genomes of the wild mulberry silkmoth, Bombyx mandarina, and its close relative, the domesticated silkmoth, Bombyx mori. Mol. Biol. Evol. 19:1385-1389.[Free Full Text]

Accepted for publication May 10, 2003.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Mol Biol EvolHome page
A. Kurabayashi, M. Sumida, H. Yonekawa, F. Glaw, M. Vences, and M. Hasegawa
Phylogeny, Recombination, and Mechanisms of Stepwise Mitochondrial Genome Reorganization in Mantellid Frogs from Madagascar
Mol. Biol. Evol., May 1, 2008; 25(5): 874 - 891.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
R. K. Jansen, Z. Cai, L. A. Raubeson, H. Daniell, C. W. dePamphilis, J. Leebens-Mack, K. F. Muller, M. Guisinger-Bellian, R. C. Haberle, A. K. Hansen, et al.
Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns
PNAS, December 4, 2007; 104(49): 19369 - 19374.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. Dowton
Assessing the Relative Rate of (Mitochondrial) Genomic Change
Genetics, June 1, 2004; 167(2): 1027 - 1030.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow Supplementary Material
Right arrow All Versions of this Article:
20/10/1612    most recent
msg176v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (26)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Shao, R.
Right arrow Articles by Barker, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shao, R.
Right arrow Articles by Barker, S. C.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?